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ILLINOIS BIOLOGICAL 
MONOGRAPHS 


PUBLISHED QUARTERLY 
UNDER THE AUSPICES OF THE GRADUATE SCHOOL 
BY THE UNIVERSITY OF ILLINOIS 


VOLUME xX 


Urbana, Illinois 


1926 


EDITORIAL COMMITTEE 


STEPHEN ALFRED FORBES WILLIAM TRELEASE 


HENRY BALDWIN WARD 


TABLE OF CONTENTS 


VOLUME X 
NUMBERS 

1. Studies on the Avian Species of the Cestode Family Hymenolepididae. 

7 By R. L. Mayhew. With 9 plates and 2 text figures.............. 
2. Some North American Fish Trematodes. By H. W. Manter. With 6 
Platesw2icharts: and: 1 textmgures sciccls x sce cause ics tious (elaine ike mess 

3. Comparative Studies on Furcocercous Cercariae. By H. M. Miller, Jr. 
With:8: plates and:2 text figures). so s.002 02s sce crs geete ea ae 

4. A Comparison of the Animal Communities of Coniferous and Deciduous 


Forests. By I. H. Blake. With 16 plates and 25 tables.......... 


PAGES 


1-126 


127-264 


265-370 


371-520 


Digitized by the Internet Archive 
in 2011 with funding from 
University of Illinois Urbana-Champaign 


http://www.archive.org/details/comparativestudi10mill 


COMPARATIVE STUDIES ON 
FURCOCERCOUS CERCARIAE 


WITH 8 PLATES AND 2 TEXTFIGURES 


BY 
HARRY MILTON MILLER, Jr. 


P Contributions from the 
Zoological Laboratory of the University of Illinois 
under the Belt Henry B. War 
0. 290 


THESIS 


SUBMITTED AS PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR 
THE DEGREE OF DOCTOR OF PHILOSOPHY IN ZOOLOGY IN THE 
GRADUATE SCHOOL OF THE UNIVERSITY OF ILLINOIS 


1923 


TABLE OF CONTENTS 


Introduction. . 
Historical Review.. 


MMe Chad stot Uny eohiatt mbes castes aren acne inc encicien ener cnvbcveamen dames 


Nomenclature. . 


Description of Species and Comparison with Related Forms ............... 
Apharyngeal Brevifurcate Distome Cercariae............ 0.00 cee 
Cercarta elvae: Miller 1923... co. oc.s0ic tn acicgiedeisccies cosa eeesebaes 
Cercaria ocellata LaVal. St. George 1855 ........... 22 eee ee 
Cercaria bombayensis no. 19 Soparkar 1921 ................ 
Cercaria gigantea Faust 1924 ....... cece eee eee eee 
GCercaria. wards Miller 1923 ii. oioctsc ce oc ce aie. 3b yieceiels ¥ 9/6 sseleie oim) ointe 
Cercaria bombayensis no. 13 Soparkar 1921... 0... eee eee eee 
Cercaria indica XXV Sewell 1922............ 2. eee e ee eee 
Pharyngeal Longifurcate Distome Cercariae...........0. 00.000 ee eee 
Gercariasburte Wier 1923 oscar cceasyes sane oc sie tgiacye ars cvciretnia-ouatavccarapeverecits 
Cercarraidoustast Cort, 1917. ic cassisisseie gecte G oa erereGecaeeans sos 
Cercarza tenuts Miller 1923200 csc she osce se case ee evcnewe dt csom ses 
Cercaria: chrysenterica) Miller 1923 fi. cies cawcscee ices et ones oe 
Cercaria emarginatae Cort 1917... 2.0... ee eee ee eee 
Cercaria letifera Fubrmann 1916 ............-. ee eeecee ones 
Pharyngeal Longifurcate Monostome Cercariae ...........e00s00e eee 
Cercaria multicellulata Miller 1923. ............ 002s cece ee eeeeee 
Cercaria hamata Miller 1923. 0. ccnhiccce vd pice teekseeessenens 
Cercaria rhabdocaeca Faust 1919 .. 1... 0.0 ee ee eee 
(lASSifica tion ee vem tere ete sieves coors ees mre MSS ave ns Rflavar do avagialaeariava, axagareeiaySactss 
Apharynpeall Cercariaess. < o.<ccaiecnisrate nar G deen buses oe scree auc es 


Apharyngeal Brevifurcate Cercariae. . 


Apharyngeal Brevifurcate Distome Cercariae..............- 
Apharyngeal Brevifurcate Monostome Cercariae............. 
Apharyngeal Longifurcate Cercariae..... 0.0... cee eee cee eee 
Apharyngeal Longifurcate Distome Cercariae................2 00000 
Apharyngeal Longifurcate Monostome Cercariae...............-0-005 
Pharyneéal ‘Cercariaes icc ce teccaie en afave ore oie t- Syciayh wlerercrare eter'ers oe ays 
Pharyngeal Brevifurcate Distome Cercariae................. 
Pharyngeal Brevifurcate Cercariae .........-..22 0.0.00 ee eee 
Pharyngeal Brevifurcate Monostome Cercariae............ 
Pharyngeal Longifurcate Cercariae........... 002-0000 e ccc 
Pharyngeal Longifurcate Distome Cercariae................ 
Pharyngeal Longifurcate Monostome Cercariae.............. 
Furcocercous Cercariae of Uncertain Position. ................000055 


Check List of Furcocercous Cercariae.......... 00. cece cee cece ee ence 
Fresh Water Species ................--5- Se unter extyaaene Sic See RNY 
Marine: SpecieS nije c.. eae nan gai oa cineca hs Aas Mi aS actin te es 
SS VIOLINS oes at Mes atec ore yaad Sites steno a tisaeayousgreieicu stele nicee mia ere 

Discussion of Life Histories, <..<5..c0c esses cea vec or aned eran ee need se sene 

Incidence’of Infection’ of ‘Snails: 2... cs.ic0s ose code oiida sano hema ghawes bes dt beeen 
Multiple: Infections igcic.2 5 xpeteiege oytcievs se) eucie foie. chasers a,avateue viteh asic ea Alejane ss aianarcusie/ ate 

Summary ob Resultse. aaeat A aammoninn 18s pene Sek oa mite roan aes 


Bibliography 


eplancden Of Pleo gig) cloaca eevee ania 


265] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER- 7 


INTRODUCTION 


Early in the study of larval trematodes, begun in 1920 at the suggestion 
of Professor Henry B. Ward, the author’s interest became centered on the 
furcocercous cercariae, and exclusive attention was devoted to these forms. 
In this work all larvae which possess a tail with a bifurcated distal end have 
been considered, although the heterogeneity of the group is recognized and 
was, indeed, a reason for the present study; these forms are also of interest 
because of the relation of some of them to schistosomiasis. 

Collections of the common pulmonate snails, Planorbis and Physa, from 
the Drainage Ditch, Urbana, Illinois, as well as from small streams running 
into it, yielded furcocercous cercariae. Species of branchiate snails of the 
genera Goniobasis and Campeloma from several localities were also ex- 
amined, but no furcocercous infections were found. During the summer of 
1921 theinvestigations were carried onat the University of Michigan Biologi- 
cal Station at Douglas Lake, Michigan; various species of pulmonate and 
branchiate snails were collected from the waters of this region. Complete 
collection and infection records are given in another part of this paper. 

As a result of this study seven new species of furcocercous cercariae are 
added to the fauna of North America; and the author is able, from a per- 
sonal knowledge of some partly described forms, and with the advantage of 
access to recent literature, to present a survey of this group of larval trema- 
todes. 

To Professor Henry B. Ward, under whose direction the investigations 
have been carried out, the author acknowledges indebtedness for sugges- 
tions and helpful criticisms, and for the use of his extensive private library. 
Thanks are also due to Dr. G. R. LaRue, Director of the Michigan Biologi- 
cal Station, for courtesies extended during the summer of 1921, and to Pro- 
fessor Frank Smith and Curator Frank C. Baker of the University of IIl- 
inois for the identification of snail hosts. 


8 ILLINOIS BIOLOGICAL MONOGRAPHS [266 


HISTORICAL REVIEW 


Probably the first furcocercous cercaria to be described is included by 
O. F. Miller (1773) in the Vermium Terrestrium et Fluviatilium; he placed 
it in the genus Vibrio, as Vibrio malleus. There is no figure, and the de- 
scription is short, containing the following significant words: “motu literam 
Y, quiete T simulat.’”’ This form was accepted by subsequent workers as a 
cercaria. In 1794 Abildgaard described a larval trematode from Denmark 
with a tail distally bifurcated to its middle, to which he gave the name Cer- 
caria varicans. ‘This is the first record of a larva, recognized as a trematode, 
having this sort of tail. The original description is very scanty, and as no 
details of structure were added by the few subsequent workers who dis- 
cussed this form, it could not now be identified with certainty. No internal 
structures are either described or figured, which leaves in doubt the pres- 
ence or absence of a pharynx; no ventral sucker is shown. In the figures the 
furcae are about equal in length to the tail-stem. 

Nitzsch (1817) very briefly described C. furcata, a distome larva with 
relatively long furcae sharply delimited from the tail-stem; this form has 
been mentioned by a number of authors but no significant details have been 
added. Diesing (1850), in his Systema Helminthum, included Malleolus 
furcatus Ehrenberg (1838) as the only known species of distome furcocer- 
cous larva, and listed the following as synonyms: Vibrio malleus Miiller 
(1773), Zirkelthier of Eichhorn (1781), Histrionella fissa Bory (1825), Cer- 
caria furcata Nitzsch (1817), and Cercaria VI von Baer (1826). This syn- 
onymy, with the exception of Histrionella fissa, was accepted by Moulinié 
(1856), who did not recognize the genus Malleolus, but listed the synonyms 
under Cercaria furcata Nitzsch. The present author finds no evidence in the 
literature which would set aside the disposition of Moulinié; in every case 
the accounts are so meager, with an almost complete lack of description of 
internal structure, that the species could not be identified with certainty. 
Diesing, in the Systema Helminthum, placed Cercaria varicans Abildgaard 
in a new genus Cheilostomum, as Cheilostomum varicans, the type and sole 
species; Moulinié returned this species also to the genus Cercaria. 

La Valette St. George (1855) included in his monograph on larval tre- 
matodes brief descriptions of four new furcocercous forms, a brevifurcate 
monostome, Cercaria cristata, and three distomes, C. fissicauda, C. gracilis, 
and C. ocellata. He also figured C. dichotoma Joh. Miiller, said to have been 
found by Miiller in 1850 in the Mediterranean at Nice. This paper by 
Miiller does not contain any definite reference to a furcocercous larva, and 


267] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER- 9 


the figure included by La Valette St. George has been accepted by sub- 
sequent workers. C. dichotoma is the first of the few marine furcocercous 
cercariae which have been described. Filippi (1857) questioned the valid- 
ity of C. cristata, as being distinct from C. varicans. The present author is 
of the opinion that they are distinct, because the dorsal body crest, prom- 
inent in C. cristata, was not mentioned or figured by Abildgaard for C, vari- 
cans; furthermore the latter species is a longifurcate larva, while the former 
is brevifurcate. 

Diesing (1858), in a further systematic treatise on cercariae, made a new 
genus Lophocercaria to contain only Lophocercaria fissicauda, under which 
he put as asynonym Cercaria cristata La Val. St. George; there is no reason, 
stated or apparent, for such a change of specific name. Two other species 
of La Valette St. George were placed in a new subgenus, Cercaria (Schizo- 
cerca) gracilis and C. (Schizocerca) fissicauda, as well as C. (Schizocerca) 
dichotoma Joh. Miiller. He also established the genus Histrionellina to con- 
tain only Cercaria ocellata La Val. St. George, which was designated His- 
trionellina fissicauda. No significant details of structure were added to prev- 
iously described forms by the investigations of Pagenstecher (1857), 
Wagener (1866), or Villot (1875). Ercolani (1882) briefly described three 
new species, a brevifurcate monostome, Cercaria microcristata, and two 
longifurcate distomes, C. aculeata and C. minuta. Morgan (1891) reported 
the finding of one individual, which he decided was a new species of marine 
larval trematode, taken in a tow at Jamaica; while his single sketch shows a 
bifurcated tail, very small in proportion to the body, it is not known 
whether this cercaria is too aberrant to be included with other furcocercous 
forms. 

Sonsino (1892) briefly described the first fresh water furcocercous larva 
to be reported outside of Europe, Cercaria vivax sp. ing. from Egypt. Ina 
short note (1894) he indicated that there were three pairs of flame cells in 
the tail-stem of this cercaria; this is the first record of the tail flame cells, 
which are unique for the furcocercous larvae. The work of Looss (1896) 
made this the first furcocercous larva to be described with respect to the 
excretory system pattern in the sporocyst and its development in the cer- 
caria. By his studies was established the bilateral embryonic character of 
the caudal excretory tube, which is unpaired in the mature cercaria; he 
figured the presence of an island in the excretory tube at the juncture of 
body and tail-stem. The branches of the caudal excretory tube which pass 
through the bifid portions of the tail were described as opening near 
the tips. A subterminal birth-pore was described and figured at the anterior 
end of the sporocyst. The differences between the much modified oral 
sucker of C. vivax and the typical sucker of larvae without forked tails were 
clearly recognized by Looss, who also noted and described about eight 
gland cells within this modified sucker. Thus C. vivax is the first furcocer- 


10 ILLINOIS BIOLOGICAL MONOGRAPHS [268 


cous cercaria for which there is a careful and complete description. Sonsino 
(1897) briefly reported a furcocercous distome, C. bipartita, from Italy; in 
contrast to all previously described forms, it was said to develop in rediae. 

Haswell (1902) described a marine larva, which, although it apparently 
belongs to the echincstomes, has a distally bifurcated tail and an excretory 
system in the body more like the furcocercous than the echinostome 
cercariae; no flame cells or tubules were seen in the tail. Pelseneer (1906) 
described C. syndosmyae from Syndosma alba, a marine mollusc. Lebour 
(1908) studied C. dichotoma Miiller, and figured both sporocyst and 
cercaria. 

In his treatment of the trematodes of the fresh waters of Germany and 
surrounding countries Lithe (1909) briefly summarized the descriptions of 
the furcocercous larvae; of the ten fresh water species of Europe one, C. 
varicans Abildgaard, was not included. In the scheme of classification the 
monostome furcocercous larvae, which are characterized by a median dor- 
sal crest, were grouped as the Lophocercariae, and the distomes as the Fur- 
cocercous Cercariae. In the key these last were subdivided on the basis of 
presence or absence of eye-spots, the degree to which the furcae were de- 
limited from the tail-stem and whether development took place in rediae or 
in sporocysts. Brief notations of two incompletely described forms, which 
were not named, were also included. The brevity of the descriptions in 
Liihe’s work shows how incompletely these early species are known, a con- 
dition in contrast with the work of Looss on C. vivax. 

Ssinitzin (1909) studied C. ocellata and described its morphology and be- 
havior in detail. Two differentiated sets of large unicellular gland cells, 
occupying the greater part of the body, were reported for the first time in a 
furcocercous larva, an anterior group from which the contents had been 
largely dissolved out and a posterior group containing coarse granules. 
These glands, later designated salivary glands by Ssinitzin(1911),and ce- 
phalic, poison, mucus, mucin, salivary-mucin by other authors, are in the 
present paper termed penetration glands. Although seven pairs of flame 
cells were noted as being present in the body of C. ocellata, they were unfor- 
tunately omitted from the two drawings referred to, and the pattern of the 
excretory system is therefore unknown. The presence of a greatly modified 
organ in place of an oral sucker, divided into an anterior thin-walled and a 
posterior muscular portion as subsequently described for schistosome larvae 
was noted; within, gland cells were seen, later designated as the head 
gland by Narabayashi. The type of alimentary canal which opens on the 
antero-ventral surface by a capillary tube was also figured. Blochmann 
(1910), in a paper which seems to have escaped general notice, called atten- © 
tion to the fact that death resulted to several species of fish and to axolotyl 
and salamander larvae from the penetration of great numbers of C. fissi- 
cauda. Their further development was not studied. The results of compre- 


269] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 11 


hensive studies on the stages of digenetic trematodes infesting molluscs of 
the Black Sea were published (in Russian) by Ssinitzin (1911); one furco- 
cercous larva, C. discursata, was described. He proposed the term parthen- 
ita for the mature sporocyst or redia; and salivary glands for the very large 
gland cells (penetration glands) frequently occupying the greater part of 
the body, as in C. ocellata, and discharging through heavy ducts opening at 
the anterior tip of the body. 

Odhner (1911) published a brief account of some investigations which 
Looss had made on the life history of C. cristata, and included two sketches 
of that larva; the excretory tube in the tail-stem bifurcates and passes 
through each furca, but it is not shown where these branches open to the ex- 
terior. A marine cercaria was briefly described by Odhner (1911a) and be- 
lieved to be the larva of Haplocladus minor; no figures of the cercaria were 
published. Lebour (1912), in a review of British marine cercariae, objected 
to Liihe’s (1909) use of tail form in the classification of larval trematodes, 
and proposed to divide all cercariae into two primary groups, on the basis 
of development in sporocyst or in redia. Division of the British marine lar- 
val forms was made on this basis; C. dichotoma was the only furcocercous 
form considered. 

In 1912 da Silva reported a brevifurcate distome larva, C. blanchardt, 
from Brazil; this is the first record of a furcocercous cercaria from South 
America. In the brief description and microphotograph it resembles the 
human schistosome larvae, and is considered by Lutz and others to be prob- 
ably the cercaria of Schistosoma mansoni. Miyairi and Suzuki (1913; in 
Japanese) determined the infective stage of Schistosoma japonicum to be 
a brevifurcate distome larva. The same authors (1914) published descrip- 
tions of the parthenita and cercaria, together with two plates. The cercaria 
was described as possessing three pairs of large penetration gland cells, and 
the locations of five pairs of flame cells, four pairs in the body and the fifth 
in the tail-stem, were indicated. A granular mass in the modified oral sucker 
was described, and is undoubtedly the structure later designated as the 
head gland. Ogata (1914) also described the cercaria of S. japonicum. His 
report of the number of flame cells agrees with that of Miyairi and Suzuki. 
The three pairs of penetration glands were designated poison glands, and 
the alimentary canal posterior to the modified oral sucker was correctly 
figured but not recognized as esophagus and cecum. 

Cort (1914), in a preliminary report of studies on North American 
larval trematodes, described one furcocercous form, C.douthitti; the pres- 
ence of “eight large unicellular glands, which seem to be analogous tothe 
stylet glands in certain other forms” was noted. In the compiete publica- 
tion (1915) he gave a more detailed structural analysis of C. douthitti, in 
which the term cephalic glands was used for the penetration gland cells. 
Both Liihe’s (1909) and Lebour’s (1912) classifications of cercariae were 


12 ILLINOIS BIOLOGICAL MONOGRAPHS {270 


discussed and that of the former followed; Cort adopted the term furcocer- 
cous from Liihe for larvae with distally bifurcated tails, of which C. 
douthittt was the first North American form to be described. Concerning 
the group Cort stated (1915:51): ‘The furcocercous or forked-tailed cercar- 
iae are very imperfectly known. The anatomy of only a few of the known 
forms is at all well worked out and the life-history of no one of them has 
been determined. At least a dozen species have been reported as distinct, 
some of which, however, have been described very briefly in the older , 
accounts. Sufficient evidence is not available to justify any conclusions as 
to the natural or artificial character of this group.” 

Leiper and Atkinson (1915) briefly described the primary and secondary 
sporocysts and the cercaria of Schistosoma japonicum, and also included a 
record of the presence of a larva (see figure 6 of Leiper and Atkinson) 
closely resembling C. vivax Sonsino. Their account of the cercaria of S. 
japonicum differs from those of Miyairi and Suzuki (1914) and Ogata 
(1914), in that instead of three pairs of penetration gland cells they re- 
ported five or more pairs. Leiper (1915), in the reports of the Bilharzia 
Mission to Egypt, presented the results of extensive investigations of the 
causative agents of schistosomiasis. Three distome cercariae were figured, 
one from Planorbis boissyi which upon experiment proved to be the larva of 
S. mansoni, another from Bullinus which was experimentally determined to 
be the infective stage of S. haematobium, and a third very large form from 
Planorbis boissyi (see figure 46 of Leiper); no attempt was made to describe 
these larvae in detail. All have relatively short furcae without cuticular 
keels, and are further similar in the lack of pharynges and eye-spots; the 
figures indicate that in the equipment of the penetration glands the three 
forms differ. Another form, said to be very similar to C. ocellata, was found 
in three different snails; the possession of a cuticular keel along each side of 
the furcae, and of pigmented eye-spots anterior to the ventral sucker dis- 
tinctly set it off from the schistosomes. The provisional name C. bilhar- 
ziella was used. Two other forms were found, C. vivax Sonsino and C. 
jissicauda La Val. St. George; both were reported as possessing a muscular 
pharynx. As a result of Leiper’s studies, the schistosome cercariae were 
differentiated from other furcocercous forms by the lack of pharynx, of 
pigmented eye-spots, and of cuticular keels on the furcae, which are less 
than one-half as long as the tail-stem. C. bilharziella was thought to be- 
long to a genus closely allied to Schistosoma. 

Cawston (1915), in the first of a long series of short papers in which 
South African furcocercous cercariae are meagerly described and incom- 
pletely figured, reported a new species, C. secobii, from Physopsis africana. 
Linton (1915) briefly described a brevifurcate monostome from Hydroides 
dianthus, and noted its resemblance to C. cristata La Val. St. George; it is 
the first marine furcocercous larva reported from North America. In a 


271] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 13 


second paper (1915a) he recorded another larva, from Pecten irradians, 
which he found to be much like that from Hydroides; the outline sketches 
do not make it possible to arrive at any conclusion as to their identity. 
Leiper (1916), in the fourth section of the report of the Bilharzia Mission, 
gave a table of Egyptian molluscs in which the various trematode larvae, 
including the furcocercous forms, were found. Narabayashi (1916), accord- 
ing to Cort’s (1919) translation of Miyagawa (1916), designated the gland 
cells within the modified oral sucker of the cercaria of Schistosma japonicum 
as the head gland (Kopfdriise). 

Fuhrmann (1916) described a longifurcate distome, C. letifera, which 
possesses fine bristle-like hairs on the tail-stem, structures reported for the 
first time on a furcocercous larva. Yoshida (1917; in Japanese) described a 
brevifurcate distome, Cercaria G, which is figured as having a distinct phar- 
yngeal bulb, a structure previously reported only for the longifurcate 
forms; development was said to take place in rediae. Iturbe (1917, 1917a) 
published a brief description, with one diagrammatic figure, of the cercaria 
of Schistosoma mansoni in South America. He reported five pairs of flame 
cells in the body, and three pairs of large gland cells; subsequent work on 
this species by other authors is not in agreement with these findings. 
O’Roke (1917) briefly described three new furcocercous distome larvae 
from Kansas, an apharyngeal form, C. echinocauda, and two longifurcate 
larvae, C. inversa and C. quieta. LaRue (1917), from a study of two 
agamodistomes,* which he called C. marcianae and C.vergrandis,concluded, 
on the basis of staining tests with thionin and toluidin blue, that the large 
penetration gland cells secrete mucus (mucin). Faust (1917), in a pre- 
liminary paper, described C. gracillima and C. tuberistoma, longifurcate 
forms from the pulmonate gastropods of Montana. He considered the 
apharyngeal furcocercous cercariae to be‘‘undoubtedly larval schistosomes 
as demonstrated by the experimental work of Leiper (1916) and by a close 
comparative study which the writer has made on larvae and adults” 
(p. 121). 

Cort (1917), in a discussion of the homologies of the excretory system, 
added the exact pattern of that system to the description of C. douthitti, 
and noted for the first time areas in the walls of the bladder arms which 
were ciliated, organellae which in other larvae had unquestionably been 
mistaken for flame cells. In the excretory tube of C. douthitti he described 
the small island previously figured by Looss (1896) for C. vivax, and later 
designated by Faust (1919c) as the island of Cort. For C. douthitit Cort 
reported the number of penetration glands to be ten, instead of eight as 
originally found. Three new species, C. dowglasi and C. emarginatae, longi- 
furcate larvae, and one brevifurcate form, C. elephantis, were described, 


* One of these, more properly designated A gamodistomum marcianae, has been held by 
Cort (1918:130) to be the agamodistome stage of a furcocercous cercaria. 


14 ILLINOIS BIOLOGICAL MONOGRAPHS (272 


together with the excretory system pattern of the cercaria of Schistosoma 
japonicum. ‘The six furcocercous cercariae discussed were divided into 
three groups, of which the first two were assigned to the family Schistoso- 
matidae. Members of Groups I and II are characterized by the absence 
of a pharynx and by furcae definitely delimited from the tail-stem and less 
than half its length; members of Group I possess eye-spots which dis- 
tinguish them from the larvae of Group II. The third group was created to 
contain the cercariae possessing distinct pharynges and with furcae 
which are almost as long as the tail-stem and not delimited from it. The 
homologies of the excretory systems in the furcocercous cercariae were dis- 
cussed and the importance of this system as an indicator of relationship 
was emphasized. 

Cawston (1917) suggested the name C. oculata for an apharyngeal, 
brevifurcate distome with eye-spots, and C. secobiana for a longifurcate 
larva. In a subsequent paper (1917a) he again briefly described C. oculata 
and C. secobii; later still the synonymy of C. secobiana 1917 with C. secobii 
1915 was acknowledged (1917b). Faust (1918) described C. gracillima and 
C. tuberistoma in greater detail than in the first report (1917); both larvae 
were referred to the Schistosomatidae. A number of parts of the adult 
reproductive system were recognized in cell masses present in the body of 
C. gracillima; the nervous system was also described in greater detail than 
had formerly been done for a furcocercous form. The penetration glands in 
these two larvae were designated salivary-mucin glands. In discussing the 
morphology of the different systems of larval trematodes he said (p. 44) 
of the genital system: ‘“This system of organs has been the most constant 
basis of classification of adult trematodes. It is also the best specific criter- 
ion for the larvae, although a more delicate technic is required for differen- 
tiation of the genital organs in the cercaria than in the adult worm.” And 
for the nervous system, he stated (p. 55): ‘‘this study has shown that the 
nervous system of the cercaria is constant for the group to which it belongs, 
and is a definite basis for the natural classification of the groups.’’ Faust 
(1918a) described two new forms, @. gigas and C. minor; the former is pecu- 
liarly interesting in its type of excretory system. Cort’s (1917) three groups 
of the furcocercous cercariae were discussed; Faust (p. 108) held that 
“with the broadening knowledge of schistosome larvae, it seems more 
reasonable to recognize a complete series of larval forms from those with a 
pharynx sphincter (C. douglasi, C. emarginatae, and perhaps C. vivax 
Sonsino), thru those with a degenerate pharynx, with or without intestinal 
ceca (C. gracillima, C. minor), thru those without any pharynx, but with 
well-developed mucin glands (C. gigas, C. tuberistoma, C. douthitti), to the 
human schistosome cercariae.”? C. echinocauda O’Roke (1917) was also 
studied and compared with C. gigas. In a discussion of the eye-spots in 
Digenea, Faut (1918b) described those of C. gigas in relation to the ner- 
vous system. 


273] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 15 


Cort (1918a) described the excretory system of Agamodistomum mar- 
cianae, which he held to be the agamodistome stage of a furcocercous cer- 
caria; the development and conservativeness of the excretory system were 
discussed. Later (1918b) he submitted data to support his thesis that the 
furcocercous cercariae readily adapt themselves to new molluscan interme- 
diate hosts. Cawston (1918) described C. secobii as developing in rediae, 
although he expressed some doubt as to identification of the species; in 
previous publications the parthenitae had been reported to be sporocysts. 
In a later paper (1918a) he recorded a cercaria from the Transvaal with 
furcae much longer than the tail-stem, for which the name C. gladii was 
proposed. Liston and Soparkar (1918) reported the experimental determin- 
ation of a furcocercous cercaria as the larva of Schistosoma spindale of do- 
mestic cattle. Southwell and Prashad (1918) briefly criticized Liihe’s (1909) 
classification of cercariae, because it was based on purely larval structures. 

Kobayashi (1918; in Japanese) described a brevifurcate pharyngeal 
larva with eye-spots, Cercaria F, the parthenitae of which were rediae. 
Cort (1919) described in detail and carefully figured the cercaria of Schis- 
tosoma japonicum. The most striking difference between this and the pre- 
vious accounts (Miyairi and Suzuki, 1914; Ogata, 1914) is that three, in- 
stead of four, pairs of flame cells were reported for the body; Cort also found 
two ciliated areas in the distal portion of each bladder arm; all authors 
have concurred on a single pair of flame cells in the proximal region of the 
tail-stem. He adopted from Narabayashi the term head gland for the gland 
contained within the modified oral sucker, and again used cephalic glands 
to designate the penetration glands. Of these latter glands five pairs were 
described, in contrast to three pairs reported by Miyairi and Suzuki and by 
Ogata, and the five or more pairs of Leiper and Atkinson. Cort also 
included a valuable review of previous publications in the Japanese lan- 
guage. Cawston (1919) briefly described C. spinosa from South Africa. In 
another publication (1919a) he reported finding a small eye-spotted larva 
for which the name C. parvoculata was proposed. 

Faust (1919), in a survey of the described cercariae of the United 
States, recorded the change of name of C. minor Faust 1918, preoccupied by 
Lebour (1912), to C. minima. The conservativeness of the excretory and 
genital systems was discussed, and emphasis laid upon the probable greater 
value of the latter in the determination of relationships. In a discussion of 
the excretory system in several groups of the Digenea he proposed (1919c) 
formulae for the flame cell patterns as foundin the cercariae. Brief des- 
criptions of four new species of pharyngeal longifurcate larvae were also 
included in this paper: three distomes, C. furcicauda, C. quattuor-solenata 
and C. robusticauda; and one monostome, C. rhabdocaeca.. The basic groups 
of flame cells were taken to consist of either a single flame cell and its cap- 
illary, or two or more whose capillaries united and emptied into a larger 


16 ILLINOIS BIOLOGICAL MONOGRAPHS (274 


excretory tubule. The different groups were represented in the general 
formula by Greek letters, a+6+7y+6-+e, five being the largest number of 
groups present among the ten furcocercous larvae discussed. The simplest 
condition is in the cercaria of Schistosoma japonicum, in which there is a 
definite division into an anterior group of two, a, and a posterior group of 
two, 8; the distinction between anterior and posterior flame cells rests on 
whether their capillaries empty into anterior or posterior lateral collecting 
tubules. In the formulae for C. douthitti and C. elephantis there is the same 
distinction of a for anterior and £ for posterior groups; while in the Brachy- 
coeliidae, with two anterior and two posterior groups, the primed letters 
a’and £’ are used for the former and the double-primed letters a’’ and B’’ 
for the latter, when it would seem clearer from a comparative standpoint to 
use a’ and a’’, and #’ and 8’’, respectively. Where there is no evident divi- 
sion into anterior and posterior groups, as in the excretory system patterns 
of the four new species described, Faust used three, four, or five letters to 
represent the basic groups. C. emarginatae and C. douglasi (Cort, 1917) 
were included under the general formula a+$+7, although there is a clear 
division into anterior and posterior groups. 

Faust (1919a) studied Cawston’s preserved material of three partly 
known furcocercous larvae and of the cercaria of Schistosoma haematobium; 
additions were made to the previous descriptions of C. gladii, C. secobii, and 
C. parvoculata. The description of the cercaria of S. haematobium was more 
complete than any previous one. Three pairs of penetration glands were 
found, and their ducts, as well as those of C. gladii, were described as being 
capped with hollow piercing spines, structures noted for the first time in 
connection with glands of cercariae. Material of the cercaria of S. mansoni 
from Venezuela was also studied and the presence of two pairs of granular 
and four pairs of non-granular penetration gland cells noted; each of the 
ducts was found to be capped with a hollow piercing spine. The first detailed 
table for the diagnosis of the human schistosome cercariae was included. 
Lagrange (1919) very briefly reported a furcocercous cercaria in Bithynia 
tentaculata from France. Iturbe and Gonzalez (1919) published the results 
of further studies on the cercaria of S. mansoni in Venezuela. Four pairs 
of flame cells were found in the body and one pair in the tail-stem, whereas 
previously (Iturbe, 1917) five pairs had been reported for the body. Two 
differentiated sets of penetration gland cells were found and designated 
as venom and salivary glands; these correspond to Faust’s (1919a) granular 
and non-granular glands. 

Sewell (1919) described in detail an apharyngeal larva from India, C. 
indica XXX, which corresponded so closely to the cercaria of Schistosoma 
japonicum that he was not sure of the specific identity of the new form. 
Instead of the term oral sucker, Sewell employed anterior penetrating 
organ; the structural modifications from the typical oral sucker of other 


275] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 17 


larval trematodes had previously been observed in certain furcocercous 
larvae by a number of workers, notably Looss (1896) and Ssinitzin (1909), 
but no new term had been used. Lutz (1919), in a paper largely of medical 
character, used the names Dicranocercaria ocellifera and D. valdefissa for 
two larvae; microphotographs were included but no descriptions were given 
in the text. Porter (1920) studied the cercaria of Schistosoma haematobium 
and noted the presence of three pairs of penetration glands with hollow 
spines capping their ducts, thus confirming Faust’s (1919a) previous ob- 
servation. She reported finding these cercariae in both Physopsis africana 
and Lymnaea natalensis, the latter host genus is new for this larva. The 
larva of S. mansoni was found in three specimens of Physopsis africana; 
this is the first record of this cercaria from a mollusc other than of the genus 
Planorbis. Manson-Bahr and Fairley (1920), in a study of schistosomiasis 
in Egypt, briefly described the cercariae of S. haematobium and S. mansoni. 
They reported the excretory systems to be identical with that described by 
Cort (1919) for the larva of S. japonicum, but also make the conflicting 
statement that there are “‘six pairs of flame cells arranged along the margins 
of the body.”” Two pairs of large clear penetration gland cells and four 
pairs of small granular ones were described for the cercaria of S. mansoni, 
and three pairs of large cells with acidophilic protoplasm for the cercaria of 
S. haematobium. Two other furcocercous forms were briefly described and 
figured, one longifurcate pharyngeal larva (see Manson-Bahr and Fairley 
1920, Pl. III, Fig. 7) which appeared to them to be identical with C. gladii 
Cawston, and a brevifurcate form (see Manson-Bahr and Fairley, 1920, 
Fig. 5), which, although pigmented eye-spots were lacking, they held to be 
probably C. bilharziella Lieper. 

Faust (1920), in a consideration of the pathological changes in the snail 
liver resulting from infestations with larval trematodes, noted the effects of 
several furcocercous forms, C. qguattuor-solenata, C. gigas, and the cercaria 
of Schistosoma mansont; the last two species were described as having two 
kinds of penetration glands, those which are basophilic and those which are 
eosinophilic. Cawston (1920) reported the presence of a schistosome larva 
for which he proposed the name C. crispa; no detailed description was given. 
The morphology and bionomics of C. parvoculata, C. gladii and C. secobit 
were briefly touched upon. Faust (1920a) discussed the criteria for the 
differentiation of schistosome larvae, recapitulating the most important 
morphological features and stressing the absence of those characters which 
had not yet been found in this group. The emphasis earlier placed by him 
(1918, 1919) on the parts of the developing genital system for the deter- 
mination of relationships of cercariae was, for the human schistosome 
larvae, now placed on the number and character of the penetration glands. 
The distinction was made between the acidophilic or basophilic reactions 
of the protoplasm, its finely or coarsely granular nature, and the character 


18 , ILLINOIS BIOLOGICAL MONOGRAPHS [276 


of the nuclei. These glands were described and figured for the cercariae of 
S. haematobium and S. mansoni. The absence of the head-gland in these 
two species was also noted. 

Scheuring (1920) in a preliminary account reported the experimental 
determination of the life history of Sanguinicola inermis Plehn. This is the 
first life cycle of a furcocercous cercaria, other than the three human 
schistosomes and Schistosoma spindale, to be worked out in detail. The 
infective agent was described as a brevifurcate monostome larva which 
resembled C. cristata La Val. St. George. In a survey of Cawston’s in- 
completely described species of cercariae, Faust (1920b) designated C. 
spinosa and C. crispa as synonyms of the cercariae of human schistosomes, 
and C. bilharziellalunata* as a synonym of C. oculata. Porter (1920a) 
briefly described the cercaria of Schistosoma mansoni, confirming Faust’s 
(1919, 1920) findings of two differentiated sets of penetration glands, two 
pairs of large anterior cells and four pairs of small posterior cells, all opening 
through hollow spines which cap the ends of the ducts. Planorbis pfeifferi 
was now reported as the usual host, although Physopsis africana also 
harbors this cercaria. Cort (1921) studied the development of the cercaria 
of S. japonicum in mice; although the indications of sexual dimorphism of 
adult schistosomes have not yet been described in the cercariae, in this 
publication and in a subsequent discussion (1921a) on sex in the Schisto- 
somatidae references were made to a species of schistosome cercaria with 
eye-spots, from Michigan, which exhibited size differences such that Cort 
interpreted them as sexual dimorphism. 

In a paper describing a new blood fluke from turtles, Ward (1921) es- 
tablished the family Proparorchiidae and noted that its members are cer- 
tainly related to the human blood flukes, Schistosomatidae. He also stated 
that the peculiar blood-inhabiting trematodes belonging to the genera 
Aporocotyle and Sanguinicola show evident morphological likenesses to 
the Proparorchiidae. Milton (1921), in a paper chiefly of medical nature, 
severely criticized the nomenclature which had been used by various work- 
ers in describing furcocercous cercariae. Kemp (1921) briefly described, 
from preserved materials only, Cercaria B and Cercaria C, two brevifurcate 
forms from Seistan; he also indicated the presence of a larva with extremely 
long furcae obtained in Gyrazlus euphraticus in the Hamun-i-Helmand. 
Faust (1921) added caudal glands to his previous description of C. quattuor- 
solenata. 

In a preliminary report of work dealing exclusively with furcocercous 
larvae of Brazil, Lutz (1921) stated that three new species were found to 
develop into members of the genus Strigea; for these larvae he proposed 
the names Dicranocercaria molluscipeta, D. gyrinipeta, and D. bdellocystis. 


* A private communication from Cawston makes clear that this species should be de- 
signated C. bilharziellalunata nom. nud. 


277) COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 19 


Specific descriptions of them were not given. Soparkar (1921) minutely 
described the cercaria of Schistosoma spindale of India; this is the first 
account of its structure. Four pairs of flame cells were found in the body 
and one pair in the tail-stem, while the penetration gland equipment was 
found to consist of four anterior coarsely granular cells with acidophilic 
protoplasm, and six posterior in which the finely granular protoplasm is 
basophilic. A detailed table of comparison of the three human schistosome 
larvae, of the larvae of S. spindale, and of C. indica XXX was given; the 
most extensive summary yet made of the common characters of the human 
and animal schistosome larvae was also included. The term Schistocercaria 
was proposed for the furcocercous cercariae whose identity with adult 
schistosomes has been established. Soparkar (1921a) also described in 
detail four new furcocercous larvae from India. One of these, C. bombayensis 
no. 8, is especially interesting in that it appears to be a connecting 
link between the monostome and distome groups of the brevifurcate 
apharyngeal cercariae; development takes place in typical rediae which arise 
from small sporocysts. Details of the morphology of C. bombayensis no. 9, 
a pharyngeal distome larva, and of C. bombayensis no. 13 and no. 19, 
apharyngeal distomes, were presented, with figures showing the principal 
systems. Faust (1921d) described C. octadena, a brevifurcate pharyngeal 
distome larva, from preserved material, and added notes on another South 
African form, C. secobit Cawston 1915. In this paper he suggested that 
cephalic gland (Cort 1919) isa more suitable term than mucin gland (Faust 
1918). Porter’s (1921) studies on the larvae of Schistosoma haematobium 
and S. mansoni confirmed Faust’s earlier work (1919a, 1920a) on the 
morphology of these forms, as well as her own previous findings (1920, 
1920a). Yet a third genus of molluscs was said to harbor the cercaria of 
S. mansoni; a single infected specimen of [sidora tropica was found. 

Khalil (1922) presented a structural analysis of the cercaria of S. man- 
soni based on a study of living material. His report of three pairs of flame 
cells in the body, together with two pairs of ciliated areas in the lateral 
excretory ducts, differs from most previous accounts; the larger numbers 
observed by other authors may be accounted for by the assumption that 
they have mistaken the ciliated areas for flame cells. Thus the excretory 
system pattern agreed essentially with that of the only other human schisto- 
some larva for which it was knownat that time, the cercaria of S. japonicum, 
according to Cort (1919). Khalil adopted Milton’s (1921) designation of 
peri-acetabular glands for the penetration glands; a posterior set of three 
pairs was reported, although Faust (1919a, 1920a), confirmed by Manson- 
Bahr and Fairley (1920) and by Porter (1921), had described four posterior 
pairs; all agreed on the presence of two anterior pairs. Milton (1922), from 
an incomplete study of the literature, attempted to show that measure- 
ments could be used as the basis of diagnosis of the furcocercous cercariae. 


20 ILLINOIS BIOLOGICAL MONOGRAPHS i [278 


The proposed system is too artificial; furthermore, he incorrectly took 
measurements from descriptions, assigned confusing specific names, and 
made misstatements concerning structures the original descriptions of 
which were clear. Bettencourt and da Silva (1922) described in detail the 
structure of the cercaria of S. haematobium, from snail hosts naturally 
infested in Portugal. Theirs is the first authentic accound and figure of 
the excretory system pattern which agrees essentially with that for the 
cercaria of S. japonicum by Cort (1919) and of S. mansoni by Khalil (1922), 

Cort (1922) studied the escape of cercariae from their snail hosts, using 
C. elephantis emerging from Planorbis trivolvis for most of the data. Wide 
variation was found in the numbers escaping from different molluscs; 
temperature was shown to be a factor in the regulation of the number from 
any one snail. Furthermore, the cercariae of this species emerged in regular- 
ly recurring waves, once during the twenty-four hours, the time of the wave 
differing in different hosts. 

Sewell (1922), as a result of comprehensive studies of the larval trema- 
tode fauna of India, described a large number of new species, of which 
fourteen were furcocercous forms; he included the first complete survey of 
all furcocercous cercariae. The lead of Liihe (1909) in considering separate- 
ly the monostome (Lophocercariae) and the distome (furcocercous) forms 
was followed, and the composite nature of the latter group was clearly 
recognized. Practically allofthe known furcocercous forms were considered; 
seven larvae, some of which were incompletely described, could not be in- 
cluded in his groupings. In considering the excretory system pattern he 
used formulae modified from those devised by Looss (1894:68), and used 
by Cort (1919b) in the description of a stylet cercaria. Further considera- 
tion of Sewell’s classification is included in that section in the present 
paper. He also took up Faust’s (1918:108) discussion of the distome larvae, 
in which a graded series of furcocercous cercariae in the family Schisto- 
somatidae was recognized, from larvae with a muscular pharynx through 
those with a degenerate pharynx to the apharyngeal forms. This view was 
strongly contested as being too inclusive, practically making the terms 
furcocercous and schistosome synonymous. In addition to detailed de- 
scriptions of fourteen new furcocercous cercariae, Sewell described the 
miracidia of Schistosoma haematobium and of C. indica XV; he found that 
the sporocysts producing this latter species have in addition the remarkable 
power of giving rise to miracidia. He discussed the value of the excretory 
system pattern in the miracidium and in the sporocyst and redia, and used 
these data in his tables showing relationships between the various sub- 
groups of monostome and distome larvae. In discussing the line of evolu- 
tion and development of the furcocercous forms, he presented data to show 
that the Lophocerca and the Lophoides groups of monostomes are closely 
related to his Groups 1 and 2, respectively, of the distome larvae, and that 


279] COMPARATIVE STUDIES ON FURCOCERCOUS CERCA RIAE—MILLER 21 


within each of the distome groups the sub-groups could be arranged in 
progressive series. Unfortunately, these gradations are in part based on 
errors, due to incomplete and incorrect details of descriptions of other 
authors. 

Kobayashi (1922) reviewed the accounts of the cercariae from Japan, 
Formosa and Korea which had been published in the Japanese language; 
brief descriptions of the furcocercous forms were given, one of them new. 
No specific names had been ascribed to most of these, although the original 
authors had designated them by numbers or letters. Kobayashi renamed 
the ten species by letters from A through J, and gave sketches for three of 
them. Ruszkowski (1922), in a study of the life history of Hemistomum 
alatum, very briefly described the longifurcate distome cercaria which he 
obtained from experimentally infested snails. Scheuring’s (1922) complete 
report of the life history of Sanguinicola inermis described in greater detail 
the brevifurcate monostome cercaria, whose identity with C. cristata is 
held by him to be doubtful; the excretory system pattern was not reported. 
Cawston (1922c), in a note on the differentiation of certain schistosome 
cercariae, suggested the probable synonomy of C. crispa Cawston with the 
cercaria of Schistosoma haematobium. The report of Bettencourt and Borges 
with de Seabra and da Silva (1922), on the study of schistosomiasis in 
Portugal, included a description of the cercaria of S. haematobium and a 
discussion of the nomenclature of furcocercous larvae. They found what 
was thought to be a head gland; Faust (1920a) stated that this organ is 
present only in the cercaria of S. japonicum among the human schisto- 
somes. Brumpt (1922) incidentally mentioned a furcocercous larva, 
closely allied to C. fissicauda, as being the larva of a holostome of the genus 
Tylodelphis. 

Faust (1922a) described in detail C. leptoderma, a larva which has the 
same type of excretory system as has C. vivax. This new species is the first 
furcocercous larva in which the development of this system, including the 
number of flame cells, has been followed from its first appearance in the 
germ ball to the stage of development found in the mature cercaria; the 
observations of Looss (1896) on C. vivax, while otherwise complete, did not 
make clear the numbers and arrangements of the flame cells. On either 
side of the elongating germ ball of C. leptoderma the division of the single 
flame cell establishes the fundamental anterior and posterior groups, a-+f; 
then follows a trichotomy of both a and 8 elements, followed by a tri- 
chotomy of each of the resulting cells, which results in eighteen flame cells 
on either side of the mature cercaria. The complete formula was taken as 
(a)?-++-(8)*, with three indicated as the factor to represent two successive 
trichotomies. 

In a preliminary publication on the development of trematodes of 
Brazil, Lutz (1922) reported having observed a dozen species of furcocer- 


i 
bo 


ILLINOIS BIOLOGICAL MONOGRAPHS {280 


cous larvae, many of which he found to belong to the holostomids, with at 
least one schistosome. Faust and Meleney (1923) published a brief sum- 
mary of their work on the life history of Schistosoma japonicum which later 
(1924) appeared in an extensive monograph. Tanabe (1923) described a 
furcocercous cercaria which he found to develop in experimentally in- 
fected mice into a new schistosome, to which he assigned the name Schisto- 
somatium pathlocopticum. The larva, which is an apharyngeal brevifurcate 
distome, very closely resembles C. douthitti in general appearance and 
proportions, and agrees with it in the details of the excretory and digestive 
systems; it has only three pairs of penetration glands, whereas C. douthitti 
has five pairs. Infection of mice was shown to be through penetration of 
the skin by the cercariae. 

Lagrange (1923), in a study of larval trematodes from Indo-China, de- 
scribed two furcocercous cercariae; no specific names were given and there 
are no figures. One species, Schistosoma?, is a distome and is probably 
apharyngeal; from the measurements given, it is a longifurcate cercaria, 
and none of the human schistosomes are longifurcate. The other larva is a 
brevifurcate distome, but there is no indication whether a pharynx is 
present; it is one of the few furcocercous larvae which develop in rediae. 
Miller (1923), in a publication preliminary to the present paper, described 
seven new species of North American larvae, two apharyngeal brevifurcate 
distomes, and five longifurcate forms, probably all pharyngeal, of which 
two were monostomes. A classification of the apharyngeal and pharyngeal 
brevifurcate distomes was presented; a key, based largely on data 
obtainable only from living cercariae, was given to separate the groups. 
Stunkard (1923) described a number of new blood flukes from turtles and 
discussed the relationships of the Aporocotylidae from fishes, the Spiror- 
chidae from turtles and the Schistosomatidae from birds and mammals. 
He came to the conclusion that the blood flukes constitute a natural group. 
The larvae of some, and presumably all, members of the first and last 
families are furcocercous cercariae, and in view of other similarities it 
might be expected that the Spirorchidae would also develop from apharyn- 
geal furocercous larvae. 

McCormick (1923) studied the larval trematode parasitization of seven 
species of fresh water snails from Ohio. He reported finding C. echinocauda 
and C. gracillima; the present author, from an examination of mounted 
material, believes that the identification of the latter species is doubtfully 
correct. Hesse (1923) described in detail a furcocercous cercaria from 
Lymnaea peregra in Scotland. No specific name was given; the larva is a 
pharyngeal, longifurcate distome, with seven pairs of flame cells in the 
body and two pairs in the tail-stem; there are four penetration gland cells. 
Soprakar’s (1924) detailed description of a unique furcocercous form from 
India shows it to be an apharyngeal distome larva in which the genital 


281] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 23 


system is much more highly developed than in any previously reported 
form; testes and ovary are present and active spermatozoa were found. The 
excretory system is highly developed, with forty flame cells around the 
margin of the body; the capillaries were not traced. The tail-stem is unique 
in the presence of two short cross arms, proximally located; three pairs of 
flame cells empty directly into the caudal excretory tube. The intestinal 
ceca are united in the posterior part of the body. Development of this 
species takes place in rediae. 

Szidat (1924) described three pharyngeal longifurcate distomes from 
Prussia; they were not given specific names, but were designated as Cer- 
caria A, Cercaria B and Cercaria C. The question of the identity of Cercaria 
B and C. gracilis, and of Cercaria C and C. letifera, C. furcata and C. fis- 
sicauda was raised by Szidat, who felt that the incompleteness of the earlier 
descriptions made a decision impossible. Following penetration of Cercaria 
A into Lymnaea palustris and its migration to the hermaphrodite gland, 
_ its development into Tetracotyle typica Diesing was traced and several 
stages were figured. This is the first demonstration of the post-larval de- 
velopment of a pharyngeal furcocercous cercaria, although the preliminary 
report of Lutz (1922) indicated that similar results had been obtained with 
three South American forms. 

Faust and Meleney (1924) published a large monograph on oriental 
schistosomiasis, in which the results of their extensive studies from both the 
medical and zoological aspects were presented. They reported the results 
of much experimental as well as observational work which they had carried 
out on different phases of the life cycle of Schistosoma japonicum, and in- 
cluded a valuable review of the important literature, most of which had 
hitherto been practically inacessible, since it is in Japanese. Their most 
important contribution to the knowledge of the cercaria is a study of the 
excretory system development in five stages, a-e, of the schistosomulum. 
It was found that the loss of the tail-stem flame cells is compensated by the 
early division of the other flame cells draining into the posterior collecting 
tubules. In the y stage a division of each of the flame cells has taken place, 
so that there are eight in either lateral half of the body; a further dichotomy 
has taken place in the e stage, resulting in a total of thirty-two flame cells 
for the entire body. These stages show the method of systematic elabora- 
tion of the flame cell pattern in the cercaria to the excretory system of at 
least the young worm, and presumably on to the adult schistosome. This 
is the first record of excretory system development in a number of the post- 
larval stages of a furcocercous cercaria. Faust (1924), in a further study of 
larval flukes from China, described three furcocercous forms, C. pseudo- 
vivax, C, divaricata* and C. gigantea. The first two are pharyngeal longifur- 


* This larva is listedin his Table I, page 296, and in Table II opposite page 298 as C. 
divaricauda; the specific description on page 256 is headed C divaricala nov. spec. 


24 ILLINOIS BIOLOGICAL MONOGRAPHS (282 


cate larvae; although the alimentary canal of C. gigantea is unknown, in 
other respects it rather closely resembles C. bombayensis no. 19, and is 
probably apharyngeal. It is surprising that the three new larvae are in- 
cluded under the family Schistosomatidae, especially the two which have 
definite pharynges; it would seem that Faust has not taken cognizance of 
the work of Ruszkowski (1922) and Lutz (1922) on the life histories of 
holostomes, all of which, so far as known, have furcocercous pharyngeal 
larvae. Faust also considered all previous descriptions of larval trematodes 
from the Sino-Japanese regions, and assigned specific names to the cercariae 
reviewed by Kobayashi (1922). The most important part of the paper 
deals with the systematic grouping of larval and adult trematodes; this 
will be discussed in detail in this paper under the heading of Classification. 

Miller (1924) studied C. douthitti and showed that it has most of the 
typical characters of the schistosome larvae; Cort’s description was emend- 
ed in certain particulars. Studies on co-type material of C. echinocauda 
showed that a very large posterior cell mass of unknown function is present, 
as are two differentiated sets of penetration gland cells; a head gland and 
an alimentary canal similar to that of C. elvae were also described. Similar- 
ities of C. echinocauda with C. elephantis were noted. Blacklock and Thomp- 
son (1924) described the cercaria of Schistosoma haematobium from both 
living and preserved material obtained from Physopsis cf. globosa in Sierra 
Leone. Their account differs strikingly from the descriptions of Faust, of 
Bettencourt and da Silva, and of Bettencourt, Borges et al in the number 
and character of the penetration glands. Instead of three pairs of similar 
glands, they report two pairs of large anterior cells containing coarsely 
granular protoplasm, and three pairs of smaller posterior cells which are 
finely granular. Except when overwhelmed with stain, the anterior cells 
are eosinophilic, and the posterior are basophilic to Ehrlich’s hematoxylin; 
“the results obtained by staining were, however, not constant, even in 
fully developed cercariae.”’ (p. 218). These authors critically surveyed the 
descriptions of the three human schistosome cercariae and severely at- 
tacked the work of Faust on the cercariae of S. haematobium and S. man- 
soni; they have either not seen or have ignored the work of Manson-Bahr 
and Fairley and of Porter which confirmed Faust’s descriptions (in details) 
with respect to gland numbers in these two species. In support of their 
view that they are dealing with the cercaria of S. haematobium is the 
epidemiological evidence of the presence of the urinary schistosomiasis 
of this trematode and the absence in Sierra Leone of the intestinal type 
caused by S. mansoni. Furthermore, they found this cercaria in no other 
host than Physopsis sp., the genus in which the larva of S. haematobium 
in Africa has usually been found. They also reported the recovery of 
adult males morphologically identical with S. haematobium, from guinea 
pigs and monkeys experimentally infected with the cercaria described. 


283] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 25 


Their account of the experimental infection of Physopsis cf. globosa with 
miracidia, hatched from terminal-spined eggs from the urine of an infected 
case, is less conclusive, fifteen days, judging from the life history of S. 
japonicum, is much too short a period for the development of the mira- 
cidium through the parthenogenetic generations to mature emerging 
cercariae. Only nine snails were used, and of these three were later found 
to be infected; the statement that “controls which were dissected did not 
show any infections” does not indicate the number used. It seems likely 
that the three experimental snails harbored natural infections which, in 
one case, resulted in emerging cercariae on the fifteenth day. These 
cercariae developed in monkeys into adult males of S. haematobium. 

In a short paper written after studying Khalil’s (1922) description of 
the cercaria of S. mansoni and the account of the cercaria of S. haematobium 
by Bettencourt and da Silva (1922), Blacklock and Thompson (1924a) dis- 
cussed the close morphological correspondence of their species with that 
described by Khalil from Egypt as the cercaria of S. mansoni. On the 
contrary, there is variance with the description of the cercaria of S. haema- 
tobium (Bettencourt and da Silva) from Portugal. Blacklock and Thomp- 
son conclude that if the glands of the cercaria of S. japonicum are constantly 
of one type this species may be differentiated from the other schistosome 
larvae; but that the cercariae of S. haematobium (as described by them), 
of S. mansoni (according to Khalil), and C. indica XXX are without 
significant morphological differences. They discuss the possibility of classi- 
fication by intermediate host; the only well established case of the cercaria 
of S. haematobium in a mollusc genus other than Physopsis (Bullinus), that 
of Bettencourt et al in which Planorbis metidjensis in the sole carrier in 
Portugal, seems to them to make it impossible to identify the human 
cercariae by this means. This view is supported by the work of Porter 
(1920a, 1921), apparently unknown to them, in which the cercaria of S. 
haematobium in South Africa was found in both Physopsis and Lymnaea, 
and the cercaria of S. mansoni was found in Physopsis and in Isidora as 
well as in the usual host Planorbis. 


METHODS OF INVESTIGATION 


The emphasis laid upon the study of living material by Cort, Faust, 
Soparkar, Sewell and others is well placed, and the essentials of the method 
as outlined by Cort (1918c, 1919, 1922) were followed by the author in the 
study of the structure of all forms. At the beginning of the investigation 
in 1920 all snails of a collection were crushed to obtain the cercariae and 
parthenitae. The limitations of this method led to the adoption of the 
isolation of snails; this was done in suitable glass vials in a small amount of 
water; if mature cercariae are present they usually emerge from the body 
of the snail within twenty-four hours and may be detected easily with the 


26 ILLINOIS BIOLOGICAL MONOGRAPHS [284 


naked eye, or with a hand lens. By transference to a small aquarium the 
infested snail may be kept alive for some time, and a supply of living mature 
cercariae is made available by periodic confinement to a small amount of 
water in a vial. The exact percentage of infestation was determined by 
crushing all snails from which larvae were not emerging after forty-eight 
hours’ isolation. For the preparation of total mounts the mature cercariae 
were fixed by pouring them into a large amount of warm fixing fluid; 
Gilson’s mercuro-nitric, corrosive-acetic, saturated aqueous corrosive sub- 
limate, and Bouin’s fluid were used. Only such material was the basis of 
the measurements recorded. 

When no more living cercariae were needed, the snail was crushed and a 
portion of the infested tissue was carefully dissected, and the young stages 
and living parthenitae were studied; permanent mounts of these were also 
made. The study of immature larvae is an important phase of the work on 
structure, as certain parts are relatively more easily seen than in mature 
larvae. A portion of the infested organ, which is usually the digestive gland, 
was fixed for sectioning. Sections were cut four to five y in thickness, and 
stained with various standard stains. The mounting media employed were 
Canada balsam and, for total mounts, white or green Diaphane. Studies 
were also made of temporary mounts in various oils, and in glycerine and 
glycerine-and-water media, in order to secure different refractive indices. 
Intra-vitam staining with neutral red proved very useful in the definition 
of certain glands and organs, and in inhibiting the activity of the larvae. 


NOMENCLATURE 


The lack of agreement in the nomenclature of certain organs in the 
furcocercous cercariae makes it desirable to establish uniformity for future 
descriptions. A brief account of structure is presented here, based on an 
apharyngeal brevifurcate distome larva (Text-fig. 1); the various depar- 
tures from this type which are found in the different groups are included in 
the discussion. 

The structure here designated as anterior organ (ao) is a modified oral 
sucker, which Sewell (1922) called the anterior protrusible penetrating 
organ. Its poor powers of attachment, and the difference in the mechanism 
of ventral sucker (v) and anterior organ have been recognized by a number 
of investigators, although many recent ones retain the term oral sucker. 
The organ is differentiated into a thin-walled anterior part and a thicker 
walled posterior part in the brevifurcate larvae; this differentiation is lack- 
ing in many of the longifurcate forms. However, the anterior organ seems 
always to be protrusible and invertible, and represents an oral sucker 
modified for penetrating tissues. Cort (1919:498) is followed in the use of 
head gland (hg) for the group of cells designated by Narabayashi as Kopf- 
driise, which are dorsally located within the anterior organ. As this struc- 


285] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 27 


ture has no connection with the mouth, the term oral gland proposed by 
Khalil (1922) is not suitable. The head gland is present in most known 
schistosome larvae, and possibly in all other brevifurcate forms. In several 
longifurcate larvae two or more cells, similarly located, have been reported; 
the author suggests no term for these cells; they can not be designated 
properly until it is known whether they are homologous with the head- 
gland of apharyngeal brevifurcate cercariae. 


hg “Ku 
he "| 
54 


by 


The oral cavity is seldom more than a capillary tube through the an- 
terior organ. An esophagus (e) and a single cecum, or pair of ceca (c), 
constitute the remainder of the simple alimentary canal. In the majority 
of longifurcate larvae and in three brevifurcate forms, there is a pharynxat 
a variable distance behind the anterior organ; in these cases, following the 
nomenclature for adult trematodes, the portion of the alimentary canal 
between the pharynx and the anterior organ is called the prepharynx. 

A pair of pigmented eye-spots (es) may be in connection with the 
nervous system (zs); these are called simple eye-spots when they are com- 
posed of a small, but varying, number of pigment granules of different 
shapes and sizes, and compound eye-spots when there are numerous uni- 


28 ILLINOIS BIOLOGICAL MONOGRAPHS [286 


formly fine granules, arranged as a cup within which may often be seen a 
lens. Unpigmented eye-spots have been reported. 

The large unicellular glands, usually in the middle and posterior parts 
of the body, have been variously designated as salivary, poison, cephalic, 
digestive, mucus, mucin, salivary-mucin, peri-acetabular and secretory 
glands. In one group (Vivax) they are located only toward the anterior, 
and even within the anterior organ. The confusion caused by this multi- 
plicity of terms has been considered by Sewell, who adopted salivary gland, 
first used by Ssinitzin (1911) for C. discursata. The author does not con- 
sider this a suitable designation, as the term salivary gland has, in all 
groups of the animal kingdom, been used in connection with the alimentary 
canal. Neither is the frequently used term cephalic gland satisfactory, as 
it would seem to imply an anterior location, and also it is too similar to 
head gland, which signifies an altogether different structure; mucin gland 
implies a definite chemical nature, and it is not certain that mucin is 
present in these cells. All evidence shows that these glands are concerned 
with the dissolution of host tissue; in the mammalian schistosomes and in 
certain holostomes a number of authors, including Faust and Meleney, and 
Szidat, have demonstrated that these glands disappear soon after penetra- 
tion of the skin of the definitive or intermediate host, and chiefly for this 
reason the present author has designated them as penetration glands. This 
term most nearly expresses the known function of the glands, and does not 
refer them to any definite position within the body; their location varies 
considerably in the different groups of furcocercous cercariae. In the 
brevifurcate distome larvae there may be a differentiation of the penetra- 
tion glands into two sorts: anterior coarsely-granular glands (pa) which 
are oxyphilic in sections, and posterior finely-granular glands (pp) which 
are basophilic. 

Various authors have designated as either ovary or testis the mass of 
germ cells (gc); it does not seem safe to venture a prediction as to the adult 
organ represented, except where the rudiments of all parts have been 
recognized, as by Faust (1918) in C. gracillima. 

The nomenclature for the parts of the excretory system has been com- 
piled from that used by Looss, Cort, Faust and Sewell. The posterior 
median bladder, or excretory vesicle (ev), has two lateral arms which may 
pass anteriorly with gradually diminishing caliber or which may be tubes 
of uniformly much smaller diameter than is the excretory vesicle itself. 
Cort considers these lateral arms as parts of the bladder, while Faust, 
Soparkar and Sewell have desingated them as main collecting tubes, main 
excretory tubes, and main lateral collecting tubes (mt); Sewell’s usage of 
the latter term has been accepted here. Into each main lateral collecting 
tube there usually pours an anterior collecting tubule (at) and a posterior 
collecting tubule (pt). Further subdivisions into capillary tubules (ec) lead 


287] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 29 


to the flame cells. The Vivax group, the members of which have a highly 
developed excretory system, have, in addition to the lateral collecting 
tubes, a median collecting tube which joins with a branch from each of the 
laterals at its anterior end, and which divides toward its posterior end 
before entering the excretory vesicle (see C. Jeptoderma in Faust, 1922a). 
In some cercariae there are cilia in one or two places in the main lateral 
collecting tubes; the term ciliated area (ca) has been used in describing 
these (Cort, 1919). Although, as figured by different authors, the cilia may 
be in a compact tuft or may project independently into the lumen (in the 
cercaria of Schistosomum japonicum only, as figured by Cort, 1919), this 
term may be used to designate either type of ciliation. It may benotedhere 
that these structures are seen only in the instant before a cercaria goes to 
pieces due to cover glass pressure. At the junction of body and tail, the 
excretory vesicle joins the caudal excretory tube (ct), usually with a small 
protoplasmic island at the place of union. The studies of Looss (1896) on 
the development of C. vivax revealed this as a remnant of the embryonic 
paired condition of the caudal excretory tube; Faust (1917) termed it an 
eyelet anastomosis, and later (1919c) the island of Cort (2), which latter 
designation the present author has used. 

In some species the bifurcations of the tail are less than one-half the 
stem length, while in others they are equal to and in somecaseslonger than 
the tail-stem; both the pharyngeal and the apharyngeal larvae are subdi- 
vided partly on this basis into brevifurcate and longifurcate groups. The 
caudal excretory tube bifurcates with the tail, and in brevifurcate larvae 
the branches open at the tips of the furcae (ep); in other cases the openings 
are somewhere along the edge, usually midway of the furcae. In some cer- 
cariae the furcae may be laterally flattened, and in addition provided with 
a dorso-ventral extension of the cuticula; this furcal fin-fold (ff) may be 
narrow or wide, and in the latter case it is usually fluted. It has also been 
called cuticular keel and paddle edge. 


30 ILLINOIS BIOLOGICAL MONOGRAPHS [288 


DESCRIPTION OF SPECIES AND COMPARISON WITH 
RELATED FORMS 


APHARYNGEAL BREVIFURCATE DISTOME CERCARIAE 


CERCARIA ELVAE MILLER 1923 
[Figs. 19-28, 38-42] 


Host, Lymnaea stagnalis var. appressa 
Locality, Douglas Lake, Michigan (Hook Point and Bessey Creek) 
Occasion, twice, in July and August, 1921 

This cercaria is similar to those of the family Schistosomatidae in a 
number of characters. It is most closely like C. bombayensis no. 19, which 
was found once in Lymnaea acuminata from Bombay by Soparkar (1921a: 
30), who noted that it probably belonged to the ‘‘Bilharziella”’ group of 
cercariae. The description of C. ocellata La Val. St. George which was given 
by Ssinitzin (1909:314), although incomplete in some important details of 
the excretory system, indicates close relationship of C. elvae to this form 
also. C. gigantea, recently, found by Faust (1924) in China, is most closely 
similar to C. bombayensis no. 19. 

The behavior is strikingly like that of the larvae of the schistosomes 
which have been studied in this particular. The emerged cercariae sink 
slowly through the water with body down and furcae 60° to 80° apart, and 
with tail-stem generally straight; occasionally the body is somewhat re- 
curved upon the tail. Swimming is effected by a rapid lashing of the tail, 
with either body or tail in advance; the latter is more frequent. Both be- 
ginning and cessation of locomotion are abrupt and the direction is usually 
erratic; there is probably less locomotion in a straight line than Soparkar 
(1921) reported for the cercaria of Schistosoma spindale and the author 
found in C. wardi. The inchworm locomotion described for the cercariae of 
Schistosoma japonicum by Cort (1919) and of S. spindale was observed in 
numerous specimens of C. elvae; under a cover glass it takes place as follows: 
after extension of the body, the anterior organ takes hold of the substratum, 
the body is contracted, and the posterior part is rotated through about 80°; 
the ventral sucker, which therefore protrudes laterally, is placed beside the 
anterior organ and takes hold of the substratum; the attachment of the 
latter is now released, and the series of movements is repeated. The inter- 
mittent lashing of the tail which occurs is not definitely correlated with 
either extension or contraction of the body. After decaudation, which takes 
place easily in this species, the animal is able to progress by the method 
just described, but not so readily as before. Sewell noted for C. indica 


289] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 31 


XXX, apparently a true schistosome, that there was a marked tendency 
to shed the tail while under observation. This organ, when detached, 
continues in erratic locomotion for some time. When the larva is at rest, 
or practically so, the furcae are often held at right angles to the tail-stem. 

There are several additional points of behavior under a cover glass to 
be noted. The animal takes hold of the substratum with its anterior organ 
and makes slow, jerky movements of the body; or body and tail are held in 
a straight line, somewhat rigid, and then rapidly bent in the middle to one 
side and the other several times. Often there are rapid vibrations of the 
tail, such that the animal is spun around on the anterior organ as a pivot; 
less frequently, the ventral sucker is attached and acts as the center of 
turning through an angle of less than 180°, but, due possibly to the large 
size of this form and consequent greater pressure of the cover glass, there 
is no complete spinning about, such as was reported by Cort (1915:50) 
for C. douthitti from Lymnaea reflexa, and has been observed by the pre- 
sent author for the same form from L. stagnalis var. appressa when studied 
under a cover glass. 

Sizes under various conditions are: maximum extension when living, 
body 368 yp by 80 y, tail-stem 501 yw, furca 328 uw; well-extended specimens 
mounted in Canada balsam (average), body 368 yu by 41 yu, tail-stem 382 u, 
furca 290 wy. Although both C. bombayensis no. 19 and C. ocellaia are larger 
than C. elvae, the proportions in length of body, tail-stem, and furcae re- 
main practically constant; the tail-stem is somewhat longer than the body, 
which in turn is longer than the furcae. C. gigantea is smaller than any of 
these three. 

C. elvae is very transparent; the deeply pigmented eye-spots stand out 
in sharp contrast to the hyaline body of the living animal, and the thick 
ducts of the penetration glands are very prominent structures, especially 
from the region of the eye-spots forward and through the anterior organ. 
The spindle-shaped body tapers more gradually from the ventral sucker 
toward the anterior end than toward the posterior; it is the contraction 
and extension of the anterior part of the body which cause the great changes 
in length. Because of the protruding ventral sucker a frontal mount is 
difficult to obtain, and the cercaria is usually seen lying on its side, in 
which position practically all observations must be made. 

The entire surface is evenly and finely spined; Soparkar showed a like 
condition for C. bombayensis no. 19. For C. ocellata, sensory hairs were 
reported on the body and ends of the furcae; it is possible that Ssinitzin 
mistook the flutings of the furcal fin-folds for hairs, as O’Roke did later on 
C. echinocauda (1917); the latter error was corrected by Faust (1918a). 
C. gigantea is spined on body, tail-stem and furcae. 

The anterior organ is large, and occupies the entire anterior third of 
the body; the length in mounted specimens averages 96 yw. Its shape is 


32 ILLINOIS BIOLOGICAL MONOGRAPHS [290 


pyriform in the living animal, with the small end posterior (Fig. 22), and 
elongate-oval or dumb-bell shape in mounted cercariae. The walls of the 
posterior part are strongly muscular (Fig. 28) as in the known schistosome 
larvae, and as in C. ocellata and in C. bombayensis no. 19. The anterior 
part is thinner (Fig. 26), especially toward the foremost part which is, as 
Cort reported for the cercaria of Schistosoma japonicum, in direct contact 
with the cuticula (Fig. 27); the same condition is present in C. ocellata and 
C. bombayensis no. 19. The head gland is conspicuous in the anterior organ; 
its size varies, but it never extends far into the posterior muscular part. It 
appears coarsely granular in the living animal and is strongly eosinophilic 
in sections. Ssinitzin observed in C. ocellata what was probably a head 
gland; such an organ is present in C. bombayensis no. 19 and in C. gigantea. 
Whether it consists of one cell or many has not been definitely determined. 
Large nuclei are seen in both total mounts and sections; it could not be 
observed whether they are enveloped by the head gland wall or merely 
pressed against its surface. Cort noted for the cercaria of Schistosoma 
japonicum that ‘‘a layer of large nuclei surround the gland and are evi- 
dently a part of it.’”’ Soparkar, in his description of the larva of S. spindale, 
was less confident of the relations, and stated that “‘it is surrounded by 
several nuclei, but these do not seem to be a part of the gland.” The open- 
ing is on the extreme anterior end, slightly dorsal. 

The ventral sucker is prominent; it has a diameter of about 33 uw in 
living larvae and averages 23 yw in specimens mounted in Canada balsam. 
There are at least two sets of muscle fibers: circular ones are especially 
prominent around the non-nucleated distal part (Fig. 21), while powerful 
bands radiate from the proximal region to parts of the dorsal side of the 
body, where they are inserted. These bands are very clearly seen in the 
living animal and are more striking structures in this cercaria than in any 
other form observed by the author. 

The powerful tail is attached terminally to the body; it is about as wide 
as the body at its proximal end and diminishes slightly toward the end 
where the two furcae arise. These are not so sharply delimited as in the 
larvae which are known to be true schistosomes, but represent an inter- 
mediate condition between them and the longifurcate forms. The furcae 
of C. ocellata are shown with constrictions at their bases by both La Valette 
St. George and Ssinitzin; Soparkar does not so figure them for C. bombay- 
ensis no. 19. There are four large bands of longitudinal muscles, and two 
small ones which apparently consist of but one fiber each (Fig. 23). The 
furcae are somewhat laterally compressed. 

The eye-spots of C. elvae are compound; each is a cup, composed of fine 
brownish granules, within which a lens is found (Fig. 39). The average 
measurements are 8 » wide and 5 pu deep, and the greatest diameter of the 
protruding lens is about 5 uw. It is evident that the same type of eye-spot is 


291] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 33 


present in C. bombayensis no. 19; Ssinitzin’s account for C. ocellata is not 
absolutely clear on this point; Faust described a pair of pigmented eye- 
spots in C. gigantea, as well as pigmentation on the body. 

The type of alimentary canal is similar to that found in the schisto- 
somes, with a small ventral mouth, a capillary esophagus through the 
anterior organ (Fig. 28), penetrating its wall in the posterior median 
region, and continuing (Fig. 41) to bifurcate into short ceca. In the cer- 
cariae of Schistosoma japonicum and S. spindale the ceca are represented as 
heart-shaped, somewhat variable; at the most they are short dilated 
diverticula. In both C. elvae and C. ocellata they are short and straight 
(Fig. 20), differing only in length from those of C. bombayensis no. 19, in 
which they are curved partly around the ventral sucker, terminating at 
about its middle. The difficulty of observing the presence of the mouth and 
oral tube, especially in preserved material, is considerable, even with a 
magnification of 1380 diameters; Ssinitzin noted the same difficulty in 
C. ocellata. Faust was unable to find an alimentary canal in C. gigantea. 
No trace of a pharynx is found in any of these forms. 

The main part of the nervous system is represented by a bilobed mass 
which lies just anterior to the eye-spots, in connection with it (Fig. 19). 
In C. bombayensis no. 19 two large lobes lateral to the penetration gland 
ducts were observed, without a cross-connection; in C. e/yae the penetration 
gland ducts of each side pass directly under the ganglionic mass (Fig. 41). 
These ducts are median to the lobes of the nervous system also in the 
cercariae of Schistosoma spindale and of S. japonicum. 

The penetration glands occupy a great part of the body, almost the 
entire posterior half of C. elvae, and even a considerably greater portion of 
C. ocellata. Furthermore, there is a definite distinction in each between an 
anterior and a posterior group of cells. On the contrary, these glands in C. 
bombayensis no. 19 and C. gigantea are less prominent structures, and no 
distinction of two sets is shown. Under low magnification, the body and 
tail of C. elvae are transparent, and slightly yellow in color, with the ex- 
ception of the greater part of the body posterior to the ventral sucker, 
which is a clear light gray. Around the ventral sucker there is a yellow, 
more granular area representing the anterior set of penetration glands 
(Fig. 25). The number and relation of the cells within each group are not 
easily determined in the living animal, due to their transparency and con- 
tiguity, and it is only under magnification of about a thousand diameters 
that the outlines are visible. There are three pairs of clear grayish glands 
in the posterior part of the body and two pairs of circum-acetabular glands 
with more granular contents; of the latter one is anterior and the other 
posterior to the ventral sucker. In unstained specimens mounted in Canada 
balsam the grayish glands become very dark and stand out in marked con- 
trast. The ducts from these five pairs of cells run forward in a bundle on 


34 ILLINOIS BIOLOGICAL MONOGRAPHS [292 


each side, most prominent just anterior to the eye-spots. In lateral view 
of the living animal there are two yellow granular ducts from the anterior 
cells, dorsal to an apparently single transparent grayish duct; this latter 
is composed of three which drain the posterior cells (Fig. 39). Both cells 
and ducts of the two groups differ in staining reactions; the posterior take 
a very deep stain with Delafield’s hematoxylin and then appear coarsely 
granular; the anterior are practically chromophobic to both hematoxylin 
and the eosins, and the greater part of the contents appears to have been 
discharged, or dissolved out at some stage in the preparation. 

C. ocellata and C. elvae are not quite identical in their penetration 
gland equipment; the fact that C. bombayensis no. 19 and C. gigantea have 
only one set of four pairs of similar cells does not, in view of other characters, 
preclude their being placed with these two. For, among the larvae which 
are known to be schistosomes, the cercariae of Schistosoma japonicum and 
S. haematobium were described as having only one group of acidophilic 
glands, while Faust (1920a) showed that even in the immature larva of S. 
mansoni two sets have been differentiated, the anterior composed of four 
coarsely granular acidophilic cells, and the posterior of eight, smaller and 
basophilic. Soparkar definitely described the ends of the penetration gland 
ducts in C. bombayensis no. 19 as being capped with hollow piercing spines; 
in C. elvae spines are present, but whether they are hollow was not defin- 
itely determined. Ssinitzin did not record their presence in C. ocellata, and 
Faust made no mention of them in C. gigantea. 

The details of the excretory system were worked out in the living ani- 
mal (Fig. 20). There are six pairs of flame cells in the body; three on each 
side empty into the anterior, and three into the posterior collecting tubule. 
There is a seventh pair in the proximal region of the tail-stem. There is 
practical identity with C. bombayensis no. 19, with only minor differences 
such as locations of flame cells and length of tubules. The excretory vesicles 
are of the same type; and an island of Cort is present at the junction of body 
and tail. The caudal excretory tube bifurcates at the origin of the furcae, 
each branch passing to the tip. The bulbous expansions which project 
beyond the furcal tips in C. bombayensis no, 19 are absent in C. elvae (Fig. 
24). The main collecting tube in the latter is more nearly an arm of the 
excretory vesicle, and its lateral bending is more anterior; just before giving 
off the anterior and posterior collecting tubules there are two dilations, in 
each of which is found a ciliated area. The details of the excretory system 
n C. ocellata were not completely worked out by Ssinitzin; he noted seven 
pairs of flame cells and a small pear-shaped excretory vesicle. Unfortu- 
nately the flame cells were not shown in the figures to which he referred, 
and the text statement appears to have escaped the notice of Sewell, who 
assumed an excretory system similar to that of Cercariae indicae XXV and 
XXXVI and established an “‘Ocellata” group to include the three forms. 


293] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARI[AE—MILLER 35 


The group must be set aside and other disposition made of the members. 
The excretory system in C. gigantea was not completely analyzed. 

The principal mass of cells which in part represents the reproductive 
system of the adult is located posterior to the ventral sucker. A similar 
mass was shown in C. ocellata, C. bombayensis no. 19 and C. gigantea. It 
has not been possible to trace definitely other scattered germ cells in C. 
elvae. 

The two snail hosts both died and disintegrated during the author’s 
enforced absence from the laboratory, so that the description of the par- 
thenitae of C. elvae is lacking. One of eight large specimens of Lymnaea 
stagnalis var. appressa collected in Hook Point Cove, Douglas Lake, Mich- 
igan, on July 8, 1921, was infected; the second host was in a collection of 
twenty-three snails of the same species and variety from Bessey Creek on 
August 4, 1921. 


CERCARIA WARDI MILLER 1923 
[Figs. 29-37, 43-45, 50-54] 


Host, Planorbis trivolvis 
Locality, Urbana, Illinois (old stream bed and pool) 
Occasion, three times in April, 1921 


This cercaria is less like the members of the schistosome group than is 
C. elvae. The forms which it resembles most closely are C. bombayensis no. 
13 and C. indica XXV. All three possess a unique posterior gland, which 
in C. wardi reacts in such a way as to make it probable that the contents 
are of a mucin nature (Mathews, 1920:323; Hawk, 1921:112); the other 
two have not been examined in this regard. 

This larva is readily visible to the naked eye when swimming about in a 
small glass container; although quite transparent, the rapid vibration 
makes it seen even in somewhat turbid water. The general type of spas- 
modic, intermittent locomotion common to most of the furcocercous cer- 
cariae is found; however, C. wardi has not been observed to swim with the 
tail forward. While sinking through the water, the tail is usually bent 
around so that the animal has, with variation, the shape of a horse-shoe. 
When cercariae have freshly emerged from the snail, the touching of any 
surface is sufficient to initiate rapid darting movements. Sometimes they 
creep upon the bottom, attaching alternately the anterior organ and the 
ventral sucker; this method of locomotion is not frequently employed, 
although fairly rapid progress can be made. When cercariae are kept in a 
stender dish for some hours, the periods of quiescence upon the bottom 
become lengthened; in the great majority of cases the animal is curledabout, 
varying from a wide horse-shoe to a form in which the anterior end of the 


36 ILLINOIS BIOLOGICAL MONOGRAPHS [294 


body lies upon some part of the tail. Often the furcae project upward; 
when they, or any part, are touched with a needle or by another swimming 
cercaria, rapid locomotion is resumed. This is effected by rapid vibration 
of the whole animal, especially of the tail; however, progress does not neces- 
sarily accompany vibration; there is a node at the origin of the furcae and 
another at the junction of body and tail, and when the anterior organ is 
attached there is a third node at this point. 

Some simple experiments on viability were carried out. An infected 
snail was placed in a small stender dish containing water of the stream in 
which it had been found; after about twenty cercariae had emerged, the 
snail was successively placed in stender dishes filled with tap waterand with 
distilled water, and each was covered with a ground glass top. Observa- 
tions were made several times daily. At the end of nine hours all the cer- 
cariae in distilled water were dead, and fifty per cent were decauded. At 
the end of two days those in stream and in tap water appeared to be normal; 
dead animals were observed for the first time on the morning of the third 
day. Some were alive at the end of four days, although none lived much 
longer. It is quite evident that their viability is very low in distilled water, 
and it would seem that emerged cercariae may be kept equally well in 
stream or tap water. It is possible that under more favorable conditions 
the length of life of some individuals after emergence might be considerably 
greater than four days. In this connection it may be noted that the human 
schistosome larvae are generally said to survive about forty-eight hours 
after emergence. 

Sizes under various conditions are: maximum extension of a living cer- 
caria, body 467 y, tail-stem 730 y, entire tail 935 uw; well-extended speci- 
mens which had been mounted in Canada balsam for two years (average), 
body 243 p by 69 y, tail-stem 564 y, furca (to extreme tip of fin-fold) 202 yu; 
unstained cercariae recently mounted in Canada balsam (average), body 
265 p, tail-stem 682 » by 50 yp, furca 273 p. Body width is not easily de- 
termined, due to the irregular outline presented; in occasional specimens 
which showed a dorsal view in the freshly mounted material the body 
averaged 75 w wide. C. wardi is somewhat smaller than either C. bombayen- 
sis no. 13 or C. indica XXV, but in all three the proportions of body to 
tail-stem to furcal length are practically identical. 

There is a prominent ventral sucker, located somewhat posterior to the 
middle of the body; it almost always protrudes decidedly, and therefore a 
lateral view is the one usually obtained under a cover glass. Its greatest 
diameter measures 28 »; when completely everted, it has a rounded cone- 
shape (Fig. 34), and a cap of small spines extends about 20 » back from 
the tip. C. bombayensis no. 13, which Soparkar noted to be often seen 
lying on its side, and C. indica XXV also have prominent ventral suckers. 


295] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 37 


The entire surface of the animal is covered with fine spines, except that 
part of the anterior organ which is protrusible; this agrees with the descrip- 
tion for C. indica XXV. Because of confusion in Soparkar’s use of the word 
tail, just what the exact condition is in C. bombayensis no. 13 is not clear. 
In most of his descriptions he distinguishes between tai] and furcae, or 
furcal ramt; but in illustrations the parts of the tail are labelled stem of tail 
and furcal rami. Another example of the confusion is in the case of C. 
bombayensis no. 19, where the figure shows both tail-stem and furcae to be 
spined, and the description states that the body and ¢éail are covered with 
spines; here fail is evidently meant to include both parts, although in the 
preceding sentence tail and furcae are used. In the drawing of C. bombayensis 
no. 13 the furcae are shown without spines; the statement is, ‘both the 
body and the tail are covered with spines and the furcal rami have a thin 
membrane attached to them.” It is probable that spines are not present 
on the furcae, both because they are absent in the figure, and because tail 
has been usually used for tail-stem. The spines on the ventral sucker of 
C. wardi are larger than those on the cuticular surface; those on the anterior 
organ are small, retrorse, and very closely set together in diagonal rows, so 
as to give the appearance of the surface of a fine file. 

The anterior organ is not distinctly divided into a thin-walled anterior 
and a muscular posterior part, although it is furnished with circular muscles 
in the latter region (Fig. 32). The head gland is median and dorsal (Fig. 43), 
and varies somewhat in size in different individuals; its exact nature has not 
been determined, but it is apparently more similar to that of C. bombayensis 
no. 13 than of C. indica XXV. In the latter two large refractile cells were 
noted, with clear nuclei, and apparently with ducts opening anteriorly: 
whether these cells are equivalent to the head gland in schistosome and 
nearly related larvae is a matter for further investigation. 

The tail-stem is more than twice as long as the body; it is firmly at- 
tached, as decauded specimens are rarely met with. It has prominent 
muscles passing spirally around the proximal part, which straighten grad- 
ually until in the distal third they are parallel to the longitudinal axis. 
This condition exactly duplicates that found in C. indica XXV. The 
muscles are distributed in four fields (Fig. 45); there is a central area of 
large cells in the tail-stem which appear quite clear, and the caudal ex- 
cretory tube passes through the center. The furcae are delimited from the 
tail-stem and are furnished with wide and thin dorso-ventral fin-folds (Fig. 
51). What appear to be thickenings are seen at irregular intervals and are 
due to fluting (Fig. 44). 

There is a large H-shaped nervous system lying behind the anterior 
organ and extending forward somewhat on each side of it; the compound 
eye-spots are posterior to it, about two-fifths of the body length from the 
anterior end. Each is composed of a number of large brown-black granules 


38 ILLINOIS BIOLOGICAL MONOGRAPHS [296 


arranged to form a cup, with the open side dorso-lateral (Fig. 52). In 
living cercariae they appear almost spherical, 13 w by 15 yw, and lie in a 
clear area 22 uw in diameter. No similar pigment was observed in any other 
part of the body. Soparkar did not describe the nervous system of C. 
bombayensis no. 13; the eye-spots in this form are composed of dark gran- 
ules, and there is a refractile lens in the center of the mass. C. indica XXV 
has an irregular mass of nervous tissue anterior to the salivary gland cells 
and dorsal to their ducts; the eye-spots are in contiguity with its anterior 
surface, in contrast to their posterior location in C. wardi. That the latter 
condition is more usual is supported by the statement of Faust (1918), 
“the eye-spots of the binoculate species are usually in direct connection 
with the posterior dorsal nerve trunks.’’ However, in C. gigas (Faust, 
1918b) and in C. douthitti (Cort, 1915) they are connected with the anterior 
rami. 

The mouth is a small opening on the ventral surface of the anterior 
organ, about 22 uw from the tip; the esophagus passes through the anterior 
organ close to the ventral wall, and penetrates the posterior wall. From this 
point the esophagus passes ventral to the eye-spots, enlarges, and bifurcates 
into large ceca, the length of which varies somewhat in different individ- 
uals. There is no trace of a pharynx. 

At least three different kinds of glands are present; the ordinary type of 
penetration glands encountered in the schistosomes and nearly related 
larvae will be considered first, after which the posterior mucin gland, so far 
reported for only the three larvae discussed here, will be described. There 
are two sets of penetration gland cells, an anterior group of four, and a 
posterior group of six. It is clearly seen in the living animal, as well as in 
sections, that the protoplasm of the anterior cells is coarsely granular, 
while that of the posterior is very fine (Fig. 50). The distinction is further 
seen in the staining reactions; the former group is eosinophilic, and the 
latter basophilic to Delafield’s hematoxylin; when hematoxylin is used 
alone, the anterior cells are chromophobic. In general, then, these two sets 
of glands are similar to those in certain of the schistosomes and allied 
forms. Faust (1921d) stated that ‘‘a comparative study of the effects of 
these glands on host tissues indicates that basophilic and acidophilic glands 
are complementary in function and that a larva possessing the two dif- 
ferentiated types can penetrate the host much more effectively than one 
possessing one type. The schistosome cercariae are notable examples of the 
dimorphic type of staining reaction.” This last sentence seems to the 
author to be unjustified, in view of the fact that of the five cercariae known 
to be the larvae of schistosomes, namely those of Schistosoma japonicum, 
S. haematobium, S. mansoni, and S. spindale and Schistosomatium pathlo- 
copticum, only the first three were described at the time of Faust’s writing; 


297] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 39 


and of these only the larva of S. mansoni had been reported to have two 
sets of glands (Faust, 1920a). The larva Of S. spindale (Soparkar, 1921) 
was subsequently described as having an anterior group of four eosino- 
philic cells, coarsely granular, and a posterior set of six with slightly larger 
nuclei and finely granular or almost homogeneous protoplasm; with intra- 
vitam staining the anterior cells remain unstained and the posterior stain 
deeply. This reaction was not studied in C. wardi or C. elvae. The ducts 
from the two groups of gland cells pass ventral to the alimentary canal, 
eye-spots, and nervous system (Fig. 52), and enter the anterior organ 
ventro-laterally just at the junction of its two regions. They then continue 
through the substance of this organ and open at the anterior tip, probably 
through spines which cap the duct openings; these are seen only with 
difficulty in stained specimens. 

The posterior mucin gland is of particular interest (Figs. 36, 37). What 
are probably homologous structures have been reported for C. indica XXV 
and for C. bombayensis no. 13. For the former Sewell stated: ‘‘Behind these 
cells is a large and somewhat horse-shoe shaped mass of finely-granular 
protoplasm in which I was unable to detect any cell outlines, nor could I 
see any corresponding ducts, but I take it to be the posterior part of the 
salivary gland.”’ Soparkar described, behind the rudimentary genital sys- 
tem, ‘‘a large irregular cell with coarse granules which takes a deep stain 
when colored by the intra-vitam method. It is difficult tosay what function 
this large gland-like structure performs. No duct arising from it could be 
made out.”’ In living C. wardi, mounted in water and examined by trans- 
mitted light, this posterior mass is clearly defined, and seen to be homo- 
geneously granular and somewhat yellow. Definite ducts leading anteriorly 
from it can not be clearly observed, although up to the region of the eye- 
spots, where they seem to converge, and less clearly between them, some 
of this same yellowish granular material is seen. In well-cleared specimens 
it was possible to trace these granules farther to the anterior than Sewell 
found them in C. indica XXV. Study of sections of immature forms re- 
vealed the fact that this posterior mucin gland is composed of many small 
cells, although the cell outlines are not seen in mature larvae and only an 
occasional nucleus is observed. In an attempt to determine the nature of 
this structure some specimens were killed in warm saturated aqueous 
solution of corrosive sublimate, and after washing for a few hours in dis- 
tilled water were stained with dilute thionin in one percent phenol. From 
the fact that this posterior granular gland and the lateral extensions from 
it stain reddish, while the surrounding tissue is blue, would seem to indicate 
that this is a typical meta-chromatic reaction, and that the contents of the 
gland are of a mucin nature (see Lee’s Vade Mecum, 1921:133, 391). Simple 
aqueous solutions of both thionin and toluidin blue were also employed, 
following the method of LaRue (1915), with equally good results. 


40 ILLINOIS BIOLOGICAL MONOGRAPHS [298 


There are five pairs of flame cells in the body (Figs. 30, 31), and except 
for minor details of relative position and length of capillaries the excretory 
system is identical with that of C. bombayensis no. 13; the distal part of the 
main excretory tube on each side is provided with two ciliated areas. C. 
indica XXV has four pairs of flame cells in the body and no cilia were noted 
in the excretory tubes. The island of Cort is apparently absent in all three; 
each has one pair of flame cells in the tail-stem. C. indica XXV is quite 
different also in that the caudal excretory tube is distended to equal one- 
third of the tail-stem diameter throughout the greater part of its length. In 
all three, branches pass through the furcae to open at the tips, without 
bulbous extensions. 

A single prominent mass of germ cells is present in each larva, similarly 
situated and probably representing the same organ of the adult. In spite of 
Sewell’s statement that “‘the genital organ is represented by a compact mass 
of small round cells situated ventrally, immediately behind the acetabulum 
and between the paired salivary-gland cells and the undifferentiated cell 
mass noted above,’’ it is clear, from a comparison of his figures referred to, 
that the genital mass appears to be close to the ventral sucker only when 
seen from the ventral side. This is also the case in C. wardi, the lateral 
view of which clearly shows that the mass of germ cells really lies almost 
mid-way from the ventral sucker to the posterior end of the body. The 
apparent inconsistencies are seen to be due in both cases to the body shape 
of the larva and the positions typically assumed in consequence. Although 
Sewell assumed that this germ cell mass represented the future ovary of 
the adult, the author believes that until more is known concerning the 
development of the reproductive system, and sexual dimorphism in cer- 
cariae, the definite naming of the larval fundaments is hazardous. 

The liver tissues of the infected snail are found to be filled with masses 
of sporocysts of varying length and caliber, so tangled that it is difficult to 
dissect them unbroken. They are very irregularly constricted; the diameter 
never exceeds 100 » and is about 15 yw at points of greatest constriction; the 
longest one dissected free measured 1.4 mm. The cercariae develop in 
bunches at irregular intervals within the sporocyst (Fig. 53), at the regions 
of greatest diameter; these are much more transparent than the constricted 
portions of the tube. Throughout the length are found occasional granules 
of orange-yellow pigment, and the more opaque narrow regions contain 
sufficient numbers of minute pigment granules to produce a pale yellow 
color. Upon all three occasions on which C. wardi was found the host was 
Planorbis trivolvis, from a restricted region just north of Urbana, [llinois. 
On April 6, 1921, thirteen large individuals were collected in a pool north- 
east of the cemetery; of these one harbored the parasite. From an old 
stream-bed in Colvin’s Field one in thirty-seven, collected April 7, 1921, 
was found to be infected. Another parasitized snail in a total of twenty- 


299] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 41 


nine was collected April 19, 1921, from a point farther north in the same 
stream-bed. In the first and last collections the infections with C. wardi 
were the only ones found; in the second, two other individuals were para- 
sitized with immature furcocercous forms, the identification of which was 
impossible. 


PHARYNGEAL LONGIFURCATE DISTOME CERCARIAE 
CERCARIAE BURTI MILLER 1923 
[Figs. 46-49, 55-58, 62-66] 


Host, Planorbis trivolvis 
Locality, Burt Lake, Michigan (Colonial Point) 
Occasion, once in August, 1921. 


This cercaria is similar to C. dowglast (Cort, 1917:53) which was found 
in Physa ancillaria in the same region. Dr. Cort kindly loaned several 
slides of this larva. The two are alike and unique in certain features of the 
excretory system. The general appearance of a number of swimming C. 
burti is similar to that of any other furcocercous form with long furcal rami; 
locomotion is usually upward, with tail in advance. Under a cover glass 
there is less activity than is usually seen, and the body is for the most part 
held contracted into an oval shape. With the ventral sucker attached to the 
substratum, vibrations of the tail may cause slight rotation on it as a pivot, 
but never complete turning about. Great changes in body length are pos- 
sible; the extended body is a blunt-ended cylinder longer than the tail-stem, 
which is much less contractile. 

In permanently mounted material all degrees of contraction and exten- 
sion are seen; for purposes of determining size, individuals which were 
moderately extended were chosen, and these give the following measure- 
ments (average): body 134 pw by 35 yp, tail-stem 140 uw by 26 uw, furca 157 p. 
The tail is often distorted, so freshly-made mounts in Canada balsam were 
measured, and here the diameter of the tail-stem equals or exceeds that of 
the body; maximum sizes are: body 157 uw by 34 y, tail-stem 142 yw, furca 
157 w; minima: body 88 y by 32 yp, tail-stem 113 uw, furca 139 uw. In the living 
animal under a cover glass the length of the body at extreme extension is 
240 uw, while the usual size is, body 125 y, tail-stem 165 wu, furca 181 uw. The 
sizes given for C. douglasi are, body 150 y, tail-stem 180 yw, furca 160 yp. 
These were presumably made from mounted material; the author has made 
measurements from type material of this form which practically coincide 
with Cort’s, and which give a body width of 35 » when the length is 157 y. 
The two cercariae agree in that the body, except in extreme extension in C. 
burti, is shorter than the tail-stem; in C. dowglasi the furcae are shorter 
than the tail-stem, while in C. burti they are consistently longer. 


42 ILLINOIS BIOLOGICAL MONOGRAPHS [300 


The anterior organ is short, not infrequently almost spherical, or it may 
be pyriform with either the small or the large end to the anterior. It is not 
divided into an anterior and a posterior region, nor is there the external 
constriction which usually accompanies that condition. The entire organ 
is a thin-walled sac, apparently not muscular. Its length in both cercariae 
averages 30 uw. There is no trace of a head gland in either. The ventral 
sucker, situated posterior to the mid-point of the body, is a strong organ 
of attachment. It extends up into the body and never protrudes promi- 
nently, so that a frontal view is the usual one obtained; often it is completely 
retracted into the body (Figs. 46, 49). Its circular edge is furnished with 
several rows of small spines, easily visible, which doubtless aid in attaching 
the organ to a substratum. In mounted material the greatest diameter of 
the ventral sucker of C. burti is about 25 yw, while in C. douglasi the average 
of a number of measurements is 21 yp. 

The body and tail spination agrees in general with the brief statement 
for C. douglasi. The anterior organ region is covered with blunt, rather 
large spines which become more sparse in the region immediately posterior 
to it and are absent from the rest of the body surface. The tail-stem and 
furcae are only very sparsely spined. The tail-stem is attached strictly 
posterior to the body, and the union is evidently a strong one, as decauda- 
tion takes place very late when the animal is subjected to increasing pres- 
sure under a cover glass. There is a definite annulation of the wall, no 
doubt due to the contraction of circular muscles lying just under the cuti- 
cula. In the living animal the presence of caudal glands and their ducts is 
readily detected (Fig. 66); they are also seen in many mounted specimens. 
They are variable in number and arrangement, although the four anterior 
pairs are usually symmetrically arranged around the central excretory tube. 
Toward the posterior they may be very irregular in number, shape and 
location; in some individuals there are eight symmetrical pairs, while in 
others only a few small pear-shaped celis, irregular as to size and position, 
are seen in the entire length; this lack of regularity is similar to that re- 
corded for C. multicellulata. The tail-stem has exceptionally weak muscula- 
ture; while there are four muscle fields (Fig. 59), each is apparently com- 
posed of a single fiber, which does not stand out conspicuously from the 
wall. The furcae are laterally flattened, and when not under pressure are 
held so that their thin edge is seen when looking at a dorsal view of the 
larva; upon increase of pressure they are turned so that the broad side is 
seen, which shows a sword-like shape slightly narrowed proximally. As is 
common with longifurcate forms, there is no constriction between furcae 
and tail-stem. 

The central nerve cell mass is H-shaped, posterior to the pharynx, with 
the anterior branches lateral to, and extending forward beyond it. No 


301] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 43 


pigmented eye-spots are present, nor any cells which might represent un- 
pigmented eyes. The system in C. douglasi presents no striking differences. 

The opening of the alimentary canal is terminal; the narrow esophagus 
passes through the anterior organ (Fig. 55), pierces its posterior wall, and 
continues as a short prepharynx. The pharynx is readily seen in both 
living and mounted specimens; in the former its diameter is 13 » and in the 
latter 9 uw. Posterior to the pharynx the esophagus continues to the ventral 
sucker, where it bifurcates into narrow ceca. These are ventral to the pene- 
tration gland ducts (Fig. 49) and terminate just in front of the penetration 
gland cells; the distal part of each is contiguous posteriorly with two dis- 
joined parts (Fig. 65). This condition is doubtless comparable to that which 
Sewell described for C. indica XXII. The ceca are described for C. douglast 
as extending two-thirds of the distance between the acetabulum and the 
posterior end of the body. In C. burti the walls are relatively thick and are 
chromophobic to hematoxylin and the eosins; the contents are a granular 
mass which fills the lumen and stains very deeply with eosin. 

In the living animal the penetration gland cells and ducts are seen only 
with great difficulty, even with high magnification and with oil between the 
condenser and object slide. The cells are confined to the postero-dorsal 
part of the body; there are eight of them, containing granular cytoplasm 
which is eosinophilic and vesicular nuclei which scarcely stain except for a 
prominent acidophilic plasmosome (Fig. 60). Whether the coarsely gran- 
ular nature of the cytoplasm is due to fixation is not known, as observations 
on living cercariae were unsatisfactory because of the presence of many 
small parenchyme cells. One observation on the ducts of a living animal 
showed them passing the pharynx laterally, curving to the middle of the 
body, and entering the anterior organ at its posterior end; in mounted 
material they seem to enter posterio-laterally. C. douglasi has four pene- 
tration glands. 

The excretory system indicates close relationship to C. douglasi; the 
total number of flame cells is the same in each, but their distribution is 
different. The feature in which the two cercariae are unique is in the 
presence, anterior to the ventral sucker in C. douglasi and posterior to it 
in C. burti, of a cross-commissure connecting the two main lateral collecting 
tubes (Fig. 63). The excretory vesicle lies just anterior to the junction of 
the tail and is small and oval; its long axis is perpendicular to the body 
length and measures about 12 y» in the living animal. Less frequently it is 
seen as a crescent, when the lateral arms are swollen. While Cort’s dia- 
grammatic representation was probably not intended to show excretory 
vesicle shape, his figure indicates a somewhat different form for that struc- 
ture in C. douglast. An island of Cort is present in both larvae. There is a 
tangled mass of the main lateral collecting tube at either end of the cross- 
commissure, which finally gives rise to anterior and posterior collecting 


44 ILLINOIS BIOLOGICAL MONOGRAPHS [302 


tubules. The former drains flame cells I and II, which lie anterior to the 
ventral sucker; the latter subdivides into three tubules at a point about 
two-thirds of the distance from the ventral sucker to the posterior end of 
the body. One of these fine tubules drains flame ceils III and IV, which are 
located in and lateral to the complex convolutions; another drains flame 
cells V and VI in the posterior region of the body; the third comes from the 
single flame cell in the proximal part of the tail. In comparison, there is an 
anterior set of three flame cells and a posterior set of two on each side of 
the body of C. douglasi; there are two pairs in the proximal region of the 
tail, in contrast to the single pair in C. buriz. Until there are more data on 
the development of the excretory system from the arrangement found in 
the cercaria, the closeness of relationship of two such forms cannot be pre- 
dicted. In both larvae the caudal excretory tube passes through the tail- 
stem, is attached to the distal end just between the furcae, and divides to 
continue down one half the length of each ramus to open by a simple pore 
to the exterior. 

The genital system is represented by an irregular mass of small chromo- 
philic cells (Fig. 64) located in the posterior part of the body, just behind 
and extending slightly forward between the penetration gland cells. Similar 
scattered cells are found to the anterior, but there are no definite aggrega- 
tions. 

The parthenitae are long thin-walled sporocysts, very much tangled in 
the liver mass and difficult to dissect entire. The longest piece freed mea- 
sured more than five millimeters in length, with a range of from 46 yp to 
184 w in diameter (Fig. 47). The cercariae develop in batches, between 
which the sporocyst is constricted and the walls may be quite thick; the 
lumen is continuous. Very frequently a large number of larvae, in all 
stages of development, are present in the same dilated portion. A birth- 
pore is present near the anterior end (Fig. 48). Cort did not describe the 
parthenitae of C. douglasi; the largest piece found on one of his slides was 
1.3 millimeters long and 0.19 millimeters in diameter. It resembled very 
closely those just described; no unbroken ends were found and therefore it 
is not known whether a birth-pore is present. 

This larva was found once, from a collection of Planorbis trivolvis taken 
in a swamp near Colonial Point, Burt Lake, Michigan on August 9, 1921. 
Seven out of seventy-three individuals were parasitized with C. dburtz; three 
other infections with furcocercous cercariae were found, beside two with 
echinostome and two with stylet cercariae, in the same collection. 


303] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 45 


CERCARIA TENUIS MILLER 1923 
[Figs. 59-61, 67-77] 


Host, Planorbis trivolvis 
Locality, Burt Lake, Michigan (Colonial Point) 
Occasion, once in August, 1921. 


This is a very slender-bodied pharyngeal larva. It is an interesting 
fact that it is strikingly similar to an Indian representative of the small 
group of apharyngeal longifurcate distomes, and not to any of the numerous 
pharyngeal forms. C. gladii Cawston 1918 (according to Faust 1919a: 164) 
and C. indica XXII Sewell are the only two carefully studied longifurcate 
cercariae which lack any trace of a pharynx, and it is to the latter form that 
C. tenuis is similar in many respects. 

There is nothing unique in the locomotion of C. tenuis; under a cover 
glass it progresses by taking hold alternately with anterior organ and ven- 
tral sucker, while the tail is rather passive; usually both tail-stem and furcae 
do not appreciably change their shape or length, but are held straight, with 
the furcae almost touching or each bent to the side. The sides of the body 
are usually parallel, with the posterior end square, and the anterior end 
bluntly rounded. There are no marked changes in body form except those 
of contraction and extension. The sizes under various conditions are: 
mounted in Canada balsam, well-extended (average), body 225 u by 21 p, 
tail-stem 216 uw by 21 yp, furca 207 uw; maximum extension of living animal, 
body 288 yu, tail-stem 240 y, furca 240 yp. 

The anterior organ is oval, or sometimes pyriform with the small end 
posterior; its average length in mounted material is 45 u. The wall is thin 
and non-muscular, not differentiated into anterior and posterior regions. 
The ventral sucker (Fig. 67) is about three-fourths of the body length from 
the anterior end, and averages 25 yw in diameter. There is a single row of 
twenty-two hooked spines (Fig. 71) around its edge; the spines are attached 
with the hook projecting and pointing toward the center, so that when the 
sucker takes hold of a substratum, they aid in attachment. On the body 
surface of C. tenwis there is an oral cap of spines which are rather small and 
sparsely distributed; a slight gradation is exhibited, from large in front to 
smaller toward the posterior limit of the spined area. The spines are like 
those of C. chrysenterica; the portion from a to c is embedded (Fig. 80), 
and b projects, pointing toward the posterior. The remainder of the body 
and the tail is not spined. 

The tail is attached terminally to the body, and in the living cercaria 
it is more narrow; in well-extended specimens mounted in Canada balsam 
the two diameters are about equal. Fine annulations are present through- 
out the entire length, and the cuticula is very thin; there are neither spines 


46 ILLINOIS BIOLOGICAL MONOGRAPHS {304 


nor sensory hairs. About five pairs of caudal glands are present, which do 
not differ from those found in C. burti; number, form, and arrangement are 
not constant. The usual slender outgrowths, which lead to the wall of the 
tail-stem and evidently may act as ducts, are present. The furcae are 
broadly lanceolate and terminate in sharp points, and are not delimited 
from the tail-stem. They are much more transparent than either body or 
tail-stem. 

The nervous system is represented by an irregular H-shaped mass 
located in the anterior part of the body, generally behind the pharynx; the 
anterior branches extend lateral to this organ. Eye-spots are lacking. The 
mouth is subterminal, and the esophagus (Fig. 70) leads back to pierce the 
posterior wall of the anterior organ. The prepharynx is 8 yp long; the 
pharynx is clearly outlined and its greatest diameter is 11 y in living cer- 
cariae, 8 u in mounted material. Just behind this the esophagus is dilated; 
it bifurcates into long ceca not quite midway of the body, and these pass 
around the ventral sucker to end in two disjoined but contiguous parts 
(Fig. 75). These, as in C. burti, may be interpreted as sections which have 
not yet broken through to form a continuous lumen. The esophagus shows 
regular cross striations. The wider ceca, dorsal to the penetration glands 
(Fig. 76), contain a homogeneous mass which is eosinophilic in sectioned 
material. 

The penetration glands are located in the region just anterior to the 
ventral sucker; the details of all structures in this area are obscured by 
numerous parenchyme cells. In the living animal the penetration glands 
show as a coarsely granular, grayish and ill-defined area; in a few specimens 
it is possible to see four definite cells, with rather large refractile nuclei. 
The confirmation of this comes from the study of sections, in which the 
number of the glands and their position with reference to the alimentary 
canal may be determined. The cytoplasm of these cells is chromophobic 
to Delafield’s hematoxylin in toto and in sections, and eosinophilic in 
sections. The ducts frequently appear empty, but when the contents are 
present they also are eosinophilic. They are difficult to trace except in 
sections (Fig. 70). In the region of the openings of the ducts there are 
about eight prominent spines; they are probably arranged in a semi-circle 
around the dorsal side of the mouth opening. Cercaria indica XXII was 
said to be crowned with anteriorly-directed spines. 

The presence of five pairs of flame cells in the body, in about the posi- 
tions given them (Fig. 74), can be affirmed, as well as two pairs in the tail- 
stem. The exact connections of the capillaries with the collecting tubules 
and of these with the main lateral collecting tubes, are not known beyond 
all possible question; the arrangement shown is the probable one. The 
excretory vesicle is a tripartite structure composed of a central vesicle and 
two large dilations of the proximal ends of the main lateral collecting tubes. 


305] COMPARATIVE STUDIES ON FURCOCERCOUS CERCA RIAE—MILLER 47 


An island of Cort is probably present in C. tenuis. The caudal excretory 
tube passes through the center of the tail-stem and the four flame cells are 
very close to it; after it bifurcates each branch passes through half the 
length of the furca, to open to the exterior by a simple pore on the edge. 

The genital system is represented by a mass of cells in the posterior 
part of the body, not so close to the junction of body and tail as in those 
Jarvae in which the penetration gland cells are crowded behind the ventral 
sucker. C. temwuis develops in long sporocysts, which do not exhibit the 
variations in diameter shown by those of C. wardi or C. burti; the lumen 
is more evident through the entire length, and the cercariae are not so 
definitely separated in batches (Figs. 72, 73). The cuticula of the sporo- 
cysts, like that of the larva, is very thin. A birth-pore is located near one 
end, and the opening is in a marked prominence on the surface; the canal 
through the thick wall is not always seen in total mounts, but the raised 
lips locate the opening. 

Two out of seventy-three specimens of Planorbis trivolvis collected in 
the Colonial Point Swamp, Burt Lake, Michigan, on August 9, 1921 were 
parasitized with this larva; it was in the same collection with C. burtz. 


CERCARIA CHRYSENTERICA MILLER 1923 
[Figs. 78-94] 


Host, Lymnaea megasoma 
Location, Burt Lake, Michigan (Colonial Point) 
Occasion, once in August, 1921 


This is the first larval trematode to be reported from Lymnaea mega- 
soma, which has a restricted distribution in the north central United States 
and extends far up into Canada (Baker, 1911). C. chrysenterica is a longi- 
furcate form, and is quite similar to C. emarginatae (Cort, 1917:53); the 
author received slides of this species through the kindness of Dr. Cort. 
C. letifera (Fuhrmann, 1916:389) will be included in the same group because 
of general likeness, but descriptions of the penetration glands and of the 
details of the excretory system are lacking. All three larvae have very long 
intestinal ceca, which in the first two are dilated distally and filled with 
a yellow jelly-like substance. 

The method of locomotion is not unusual; the body is pulled after the 
tail in short straight dashes, or longer erratic ones, generally upward 
through the water. Under a cover glass there may be some progress with 
the body in advance, for short distances only; the tail lashes actively. The 
cercaria may move slowly by alternate use of anterior organ and ventral 
sucker, with accompaning form changes (Figs. 92-94). 

Sizes under various conditions are: well-extended specimens mounted 
in Canada balsam (average), body 260 u by 48 uy, tail-stem 244 uw, furca 


48 ILLINOIS BIOLOGICAL MONOGRAPHS [306 


248 yw; maximum body extension of living cercaria, 384 u. These measure- 
ments are slightly larger than those given for C. Jetifera, which is in turn 
larger than C. emarginatae; however, the author’s measurement of a large 
individual of this latter species on one of Cort’s slides gave body 254 u by 
37 w, as against a body length of 160 w given by Cort. 

The body of the living animal is the shape of a spindle with the greatest 
diameter just behind the ventral sucker, and a gradual tapering from this 
point to the anterior. The anterior organ is usually pyriform, with the 
small end posterior, although it may be oval. There are not two regions as 
distinctly differentiated as in C. elvae, although the posterior part is more 
strongly muscular than the anterior; there are both longitudinal and cir- 
cular fibers (Fig. 90). In C. letifera and in C. emarginatae the anterior 
organ is of the same general shape as that just described. No one of the 
three cercariae has a head gland. The ventral sucker is about two-thirds of 
the body length from the anterior end, but its relative position varies with 
the state of contraction. It is relatively large, especially in comparison 
with its size in the schistosome cercariae; in living larvae under some pres- 
sure of cover glass it is about 45 w in diameter, while in permanent mounts 
it shrinks to 31. It does not protrude markedly from the body (Fig. 89). 
There are small spines around its edge. In C. /etifera it is smaller, and like- 
wise it is spined; in C. emarginatae its diameter is 25 in mounted specimens. 

There is an oral cap of spines like those described for C. tenuis. Behind 
these there is a small area on which small straight spines are present; this is 
followed by a short region with no spines. Between this bare region and 
the ventral sucker are eight or nine irregular bands, each composed of two 
or three rows of spines. The region around and posterior to the ventral 
sucker is uniformly covered with spines. For C. emarginatae the statement 
is made, “heaviest spination around acetabulum, with rest of body only 
sparsely covered.” Fuhrmann reported only four or five large spines on the 
anterior extremity of C. letifera. 

The tail is attached terminally to the body and is quite transparent; 
the surface of the tail-stem is finely annulated. The number of caudal 
glands varies in different individuals, from four to eight or more pairs. 
They are relatively small and do not take up a great part of the tail-stem 
cavity (Fig. 78); the usual ducts lead to the outer surface. The furcae are 
broad and flattened. 

The nervous system is represented by an H-shaped mass which extends 
somewhat to the anterior on each side of the pharynx. This system is not 
reported for C. letifera or for C. emarginatae. There are no eye-spots. 

The mouth opening is subterminal; the esophagus passes through the 
anterior organ and penetrates its posterior wall. The prepharynx dilates 
just in front of the pharynx, and the latter is about 20 w in diameter in the 
living animal, shrinking to 15 uw after preservation. The esophagus con- 


307] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 49 


tinues to about midway of the body, passing ventral to the nervous system 
(Fig. 84), and then bifurcates into ceca which approach the dorsal wall and 
gradually increase in diameter (Figs. 86, 89). The walls of the ceca are 
thick, and several nuclei are present in them; the contents within the lumen 
appear jelly-like and homogeneous, and stain deeply with eosin. From a 
study of Cort’s material of C. emarginatae, the author finds an alimentary 
canal quite similar to the one just described. It is difficult to compare it to 
that of C. letifera, as Fuhrmann’s account is incomplete and it is not clear 
as to the location of the pharynx. 

The penetration gland cells are confined to the region median and pos- 
terior to the ventral sucker; they are four in number and are readily seen 
in the living animal. One cell on either side is lateral and ventral to the 
cecum; the remaining two are median, in tandem position, and so laterally 
compressed as to be almost in contact with dorsal and ventral body walls 
(Fig. 86). In a living cercaria the protoplasm of all four cells is coarsely 
granular; after fixation there is no definite staining reaction to either Dela- 
field’s hematoxylin or to eosin, and the greater part of the contents seems 
dissolved out. The ducts of the lateral cells pass forward ventral to the 
ceca, and those of the median cells may be contiguous for a little way (Fig. 
89). The two of each side come into contact at about the level of esophageal 
bifurcation, and pass forward together, bending medially to enter the an- 
terior organ. In connection with the duct openings, there are about twenty- 
two solid piercing spines, arranged in a semicircle around the dorsal edge 
of the mouth opening; the ten median spines are somewhat larger than the 
others. In comparison, Cort’s account for C. emarginatae stated that there 
were six glands, extending into the post-acetabular region; the author’s 
examination of Cort’s material shows the cytoplasm to be coarsely gran- 
ular and chromophobic to Delafield’s hematoxylin in total mounts. Fuhr- 
mann did not include the penetration glands in his description of C, 
leitfera, 

There are nine pairs of flame cells, three anterior to the ventral sucker, 
four in the posterior region, and two in the tail-stem (Fig. 79). C. emargi- 
natae has the same number anterior tothe ventral sucker, but they form one 
group on each side, with their capillaries emptying into the larger tubule at 
one point; in C. chrysenterica flame cells I and II have apparently arisen 
from the division of a cell, and are not near III, whose capillary joins 
separately. Posterior to the ventral sucker C. emarginatae has but two 
pairs of flame cells, the capillaries of which join the posterior collecting 
tubule at the same point; it has two pairs in the tail-stem, more distally 
located than in C. chrysenterica. Fuhrmann figured none of the excretory 
system of C. letifera except the excretory vesicle outline, so it cannot be 
included in the comparison. 


50 ILLINOIS BIOLOGICAL MONOGRAPHS [308 


The genital system is chiefly represented by a somewhat wedge-shaped 
mass of cells located in the posterior end of the body, just in front of the 
excretory vesicle and between the ends of the ceca. Anterior to the ventral 
sucker and extending up toward the origin of the ceca there are two masses 
of cells which correspond in position to the vagina and cirrus pouch shown 
by Faust for C. gracillima (1918). The relation of these cell groups to the 
large posterior mass in C. chrysenterica is not clear. 

The parthenitae are long tubes of varying diameter, which exhibit 
gradual swellings in several regions, and so are unlike other sporocysts 
described which have ball-like swellings. The longest entire individual 
dissected free from host tissue measured more than 8 mm. in length, and 
was 180 yw and 60 » in greatest and smallest diameters; in one preparation 
of sections a maximum diameter of 244 uw was observed. The walls of the 
narrow regions are thicker, although a prominent lumen extends through- 
out. The anterior end is distinguished by a solid knob of small cells, behind 
which the prominent lips of the birth-pore are seen on one side (Fig. 83). 
Some sporocysts on Cort’s slides were studied; they are quite similar to 
those just described, both in the caliber of the tube and in the presence of a 
definite birth-pore with prominent lips. Fuhrmann described the sporo- 
cysts of C. letifera and figured an individual containing immature larvae; a 
birth-pore was not observed. 

C. chrysenterica was found once only, in a collection of Lymnaea mega- 
soma from a swamp near Colonial Point, Burt Lake, Michigan on August 
9, 1921. One snail out of eighteen was parasitized. 


PHARNYGEAL LONGIFURCATE MONOSTOME CERCARIAE 
CERCARIAE MULTICELLULATA MILLER 1923 
(Figs. 1-8, 17, 18] 


Host, Physa gyrina 
Locality, Urbana, Illinois (Drainage Ditch) 
Occasion, twice, in September and November, 1922 


Cercaria multicellulata is the second pharyngeal monostome larva with 
{ong furcal rami to be described, the first being C. rhabdocaeca Faust (1919c: 
338); its similarities to this cercaria and to C. hamata Miller will be con- 
sidered in the discussion of the latter elsewhere in this paper. No trace of 
an alimentary canal has been observed in this larva, but because of its 
striking similarities to C. rhabdocaeca and C. hamata the presence of a 
pharynx, obscured by the small parenchyme cells, is assumed. Another 
reason for including C. multicellulata with the pharyngeal forms is the 
number of differences between these three larvae and the only apharyngeal 


309] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 51 


longifurcate monostome, C. indica XXVII, especially with regard to the 
excretory system. 

C. multicellulata swims sporadically; rapid dashes, generally upward, 
are effected by lashing of the tail, which is in advance. Between dashes the 
cercaria sinks body first, the tail-stem is extended in a straight line with 
the body, and the furcae are spread at an angle of about 100°. It is positive- 
ly phototactic. A series of movements, probably connected with the en- 
trance of the cercaria into a host, is frequently observed under a cover- 
glass (Text-fig. 2). From a condition in which the body is somewhat con- 
tracted and the anterior end turned in (A), the generally rounded contour 
of the anterior organ is changed to a pyriform shape as it is slowly extended 
a little (B). The anterior part of the body is then quickly thrust forward; 
the fore part of the anterior organ rapidly everts and presents the large, 
anteriorly-directed spines (C). The whole is then quickly retracted, 
rounded up, and the anterior-most part in (A). This series of movements 
is frequently alternated with one in which the everted part of the anterior 


Fig. 2 


organ (C) is rapidly thrust forward again and again, without rolling in and 
rounding up when withdrawn. The anterior otgan has an attaching 
function also; it is strong enough to hold the cercaria to the under surface 
of a cover glass which is being pushed along a slide. 

Sizes under various conditions are: maximum body extension under 
cover glass but free-moving, 184 «; almost immobile from neutral red 
(average), body 170 » by 37 y, tail-stem 230 p, furca 225 yp; fixed in hot 
Gilson’s fluid (average), body 156 u by 28 yp, tail-stem 198 p, furca 147 p; 
well-extended specimens mounted in Canada balsam (average), body 
136 w by 26 yp, tail-stem 196 wu by 24 p, furca 147 p. 

When under no compression the sides of the body are parallel up to the 
region of the anterior organ, where they taper off to a blunt end. With 
great extension the whole body tapers slightly from the posterior, and the 
anterior two-thirds may be crenated in the region behind the anterior 
organ; this crenation is due to the contraction of circular muscles just 
beneath the surface. The anterior organ varies from an oval to a pyriform 
shape in changing from a position of rest to extension; infrequently it 
contracts in the middle, becoming dumb-bell shape. It is approximately 
one-fourth as long as the body, although this proportion varies, since the 
anterior half of the body undergoes moye extension and contraction than 


BY ILLINOIS BIOLOGICAL MONOGRAPHS (310 


the posterior. The anterior organ is armed with large retrorse spines ex- 
tending over somewhat less than the anterior half, behind which they are 
both smaller and more sparse, so that, with the difficulty of observation 
due to the many small parenchyme cells in the body proper, it cannot be 
said whether they extend over the entire body; there is indication of sparse 
spination in somewhat definite bands back to the level of flame cell II. It 
may be noted here that the parenchyme cells, which are refractile, make 
difficult all observations on external and internal structure. The anteriorly- 
directed spines associated with the openings of the penetration gland ducts 
will be described in connection with those organs. The spination of C. 
multicellulata is on the whole very similar to that of C. indica XXVII, 
except that, in the latter, spines are reported for the anterior end and are 
shown as extending over only half of the anterior organ. 

The cylindrical tail-stem is of less diameter than the body; the attach- 
ment is strictly posterior. Annulations, much finer than those of the body, 
are always noted; as Sewell suggests, these are due to the contraction of 
circular muscles directly beneath the delicate cuticula. The cells composing 
the wall have relatively large nuclei (Fig. 5) which quickly take a deep 
neutral red stain from dilute solution. Within the cavity of the tail-stem 
are ten to fifteen large gland cells, slightly yellowish in color and showing 
no granulation even under high magnification (1380); they are arranged 
in pairs in the proximal portion, the caudal excretory tube passing between 
them, but farther to the posterior the pairing and size of the glands become 
irregular and they may lie on but one side of the excretory tube. While 
alive, the nuclei of these cells are seen to be relatively small and granular. 
Ducts lead to the wall of the tail-stem, and apparently open between sur- 
face cells. With contraction of the tail, the glands move within the lumen 
and the most posterior may be forced into one of the furcae. There is great 
diversity among different mature cercariae from the same snail; in some 
the glands are very clearly seen, while in others the outlines are so irregular 
that they can scarcely be recognized. As noted by Cort (1915) for C. 
douthitti, they are seen only in living specimens. While not clearly ob- 
servable as such in the tail-stem of a living cercaria, four principal muscle 
bands (Fig. 6), strongly acidophilic, are seen in sections stained with Dela- 
field’s hematoxylin and eosin. On the surface there are delicate sensory 
hairs, seen only under high magnification and with proper lighting; their 
length is about three-fourths of the tail-stem diameter. No relation was 
observed between them and the openings of the caudal gland ducts. This 
is the second record of sensory hairs on the tail-stem of a furcocercous 
cercaria; they were previously reported for the distome, C. Jetifera Fuhr- 
mann (1916). The furcae of a living cercaria are about equal in length to 
the tail-stem, and are not constricted at the base; they contract more than 
the tail-stem during fixation, and therefore appear shorter in permanent 


311] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 33 


mounts. There is an irregular lumen. On the surface are small spines in 
longitudinal rows, and the distal half is furnished with a narrow fin-fold 
which does not extend around the tip of the furca, nor is it thrown into 
folds such as are so characteristic of a form like C. gigas. 

About three-fifths of the length of the body from the anterior end is 
located a pair of simple eye-spots, composed of from four to thirty black 
pigment granules of varying shape and size. The diameter of a group of 
granules composing an eye-spot is about 6 uw, and they are frequently ob- 
served, under a magnification of 1380X, to lie in an irregularly-shaped 
clear area. 

Repeated attempts were made to determine whether an alimentary 
canal is present. Only once or twice was some indication seen of a very 
narrow tube extending behind the anterior organ to a distance of about 
one-half its length; the observations were not conclusive. 

There are three pairs of penetration gland cells (Figs.5,7). The anterior 
two are separated from the other four by a compact mass of cells, and their 
ducts are ventral to the others; all six pass dorsal to the eye-spots (Fig. 17) 
before dipping ventrally in the anterior half of the body; they become small 
before entering the anterior organ, and expand in that organ. The glands 
are more easily seen by intra-vitam staining with dilute neutral red; they 
take a deep red stain, while their ducts do not stain very deeply and are 
more yellowish, indicating either that they are empty or that the character 
of the secretion changes after entering them. That such a change from cell 
to duct may occur has been suggested by Faust (1920a); both cells and 
ducts appear coarsely granular. The entire penetration gland system is 
chromophobic to Delafield’s hematoxylin in cercariae mounted in toto, 
but it is strongly eosinophilic when sections are counterstained with eosin. 
Between the openings of the ducts of the two sides there is a group of about 
twelve solid piercing spines. 

The numerous parenchyme cells in the body make it especially difficult 
to determine the locations of flame cells and the connections of their ducts. 
The exact connections of all the small tubules could not be seen, but other 
details were made out (Fig. 5). The excretory vesicle proper consists of two 
parts about equal in width, the posterior being longer than the anterior, 
from the latter, two arms branch off antero-laterally, so large as to give 
frequently the appearance of a tri-partite vesicle. These arms narrow to 
become the main lateral collecting tubes, which bend sharply forward 
around the germ cell mass, extend anteriorly for a third of the body length, 
and bend on themselves to return a little way before dividing into anterior 
and posterior collecting tubules. The anterior collecting tubule undoubted- 
ly receives the capillaries from flame cells I, II, III, and IV; the exact con- 
nections of I and II were traced, but it is not known whether IIT and IV 
join separately or constitute a pair whose capillaries unite in a common 


ILLINOIS BIOLOGICAL MONOGRAPHS (312 


on 
rs 


tubule (Fig. 1) before joining, as in C. rhabdocaeca, with the excretory system 
of which there are many similarities. The posterior collecting tubule in all 
probability drains V, VI, VII, and VIII in the body and IX and X in the 
tail; the fact that V and VI, as well as VII and VIII, lie close together 
seems to show that their capillaries may unite before entering the posterior 
collecting tubule. There is a small island of Cort, although it is not easily 
seen; it is located in a dilated portion of the posterior part of the excretory 
vesicle, at the junction of body and tail. From this point the caudal ex- 
cretory tube runs posteriorly through the center of the tail-stem, embed- 
ding itself in a mass of cells where the furcae branch off; here it divides and 
passes down each furca to open on the dorsal edge, midway to the tip. 
These openings are simple, not having the slight enlargement and pro- 
trusion frequent in mid-furcal pores. 

Either a rudimentary ventral sucker is present, or the reproductive 
organs are represented by two cell masses (Fig. 7). A poorly-defined group 
of cells, lying just behind the posterior pair of penetration gland cells 
and bounded posteriorly and laterally by the bladder and main lateral 
collecting tubes, forms the larger mass; the group of cells in this position, 
usually staining deeply with hematoxylins, has constantly been interpreted 
as a germ cell mass in furcocercous cercariae. Between the first and second 
pairs of penetration gland cells is another cell mass, quite different in shape 
and more definite in outline; the cells composing this mass are apparently 
identical with those of the posterior mass. Whether this is a proliferating 
cell mass representing a degenerate ventral sucker, or a germ cell mass, is 
not entirely clear; no connections between the two masses were observed. 
The same two cell aggregates were found in C. hamata. 

The parthenitae are elongate sporocysts of relatively small diameter, 
so much tangled in the snail liver that it is practically impossible to dissect 
out one unbroken; the longest obtained measured almost 1 cm. in length, 
varying in diameter from a few yu to 200 u (Fig. 18). Both those containing 
only very young germ balls and those containing mature cercariae are very 
motile, especially the free ends which project from the liver. The cercariae 
develop in batches, with constrictions between. The lumen is continuous 
throughout the entire length, although at the points of constriction it is so 
narrow that, in spite of rapid surging back and forth, it is likely that the 
groups remain separate while undergoing development. The free end is 
tapering and bluntly rounded, the most anterior part being translucent and 
free from pigment granules. Following this short region there is a consider- 
able amount of yellow and orange pigment, and at a short distance from the 
anterior end are found the lips of a birth-pore (Fig. 2). The emergence of 
one cercaria was observed. 

Of a collection of ninety-seven Physa gyrina on September 18, 1922, 
from the Drainage Ditch, Urbana, two were infested; on November 4, 


313] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 55 


one-half mile farther up the ditch, twelve in 177 were infested. The sizes 
of these fourteen snails varied from 11 mm. to 16 mm., greatest length of 
shell. 


CERCARIA HAMATA MILLER 1923 
[Figs. 9-16] 


Host, Planorbis trivolvis 
Locality, Urbana, Illinois (Drainage Ditch) 
Occasion, three times, September to November, 1922 


This cercaria is similar in many respects to C. multicellulata, but may 
easily be distinguished from it by the absence of eye-spots; the figures for 
the latter may be used to show certain points of structure. C. hamata is 
also strikingly like C. rhabdocaeca Faust and may be identical with it, al- 
though there are certain differences, and some structures in the former 
which are not included in the description of the latter. The general form 
of locomotion in C. hamata and C. multicellulata is the same, but with a 
hand lens it is observed that in the case of the former the anterior part of 
the body is bent toward the ventral surface in a hook-shape when the 
cercaria is sinking through the water. 

Sizes under various conditions are: under a cover glass but free-moving, 
body, 207 uw by 41 uy, tail-stem, 276 uw, furca 276 w; mounted in Canada 
balsam (average), body 179 uw by 28 py, tail-stem 248 p, furca 198 uw. It will 
be noted that in the process of making permanent mounts the furcae shrink 
more than the tail-stem. 

Although body shape is not a reliable criterion for specific differences, 
C. hamata and C. rhabdocaeca differ in this regard. The sides of the body of 
the former are parallel and its diameter is not greater than that of the tail- 
stem; also a shape is never exhibited such as Faust has shown for the latter 
cercaria. On the contrary, the body sometimes bulges anteriorly during 
contraction, and the posterior part never increases much in diameter. All 
of the measurements of the body are greater than those given for C. rhab- 
docaeca. The two forms differ also in the form of the anterior organ; in 
Faust’s species it is described as ‘‘oral sucker pyriform, with larger end 
directed inward.” C. hamata has its anterior organ in the shape of a short 
oval, and while under cover glass pressure or in permanent mounts (Fig. 12) 
it may be somewhat pyriform, it never appears as Faust figured for C. 
rhabdocaeca. The spination is similar to that of C. multicellulata. In both 
C. hamata and C. multicellulata the tail-stem is attached terminally and 
presents the same annulated appearance; it also has a constant diameter 
throughout; in these characters both species differ from C. rhabdocaeca, the 
tail-stem of which tapers markedly, and shows no annulations, 


56 ILLINOIS BIOLOGICAL MONOGRAPHS (314 


Practically the entire lumen of the tail-stem of C. hamaita is filled with 
caudal gland cells, which are therefore not so clearly defined as in C. multi- 
cellulata; they have the same clear, homogeneous appearance, slightly 
yellow, and with transparent nuclei. Sewell’s description of short lateral 
branches of the caudal excretory tube of C. indica XXVII, also for C. 
indica II, is thought by the present author to be a misinterpretation of the 
boundaries of contiguous caudal gland cells; his records are the only ones 
of such lateral branches. The three longifurcate forms under discussion 
here are united in the absence of spines on the tail-stem, in contrast to the 
presence of a number of small, backward-pointing spines with which all 
four Indian representatives of the brevifurcate monostomes are furnished 
(C. indica IX, XIII, XXXIX, LV). C. hamata has four muscle bands in 
the tail (Fig. 10), and sensory hairs like those reported for C. multicellulata, 
relatively longer, and more numerous, about fifteen on each side; these 
have not been noted for any brevifurcate cercaria. These two forms have 
spines on the furcae; they were not reported for C. rhabdocaeca. C. hamata 
does not have thin furcal edges; C. multicellulata is the only one which has 
them. 

Various degrees of development of the alimentary canal are represented; 
C. multicellulata shows only a trace of a narrow tube posterior to the an- 
terior organ, although it is supposed that a pharynx is present, but is 
masked by the small parenchyme cells. C. rhabdocaeca was shown with a 
relatively wide prepharynx, slightly muscular pharynx, short inconspicu- 
ous esophagus, and single median cecum extending backward almost to the 
level of the first penetration gland. C. hamata has a capillary prepharynx, 
10 w long, and esophagus and cecum are represented by a pyriform vesicle 
behind the weakly muscular pharynx; the pharynx is 10 pw wide. 

The number of penetration glands in the three North American species 
is the same, although their locations are somewhat different. In both C. 
multicellulata and C. hamata the anterior cell mass (rudimentary ventral 
sucker or germ cell mass) definitely separates the six gland cells into 
two groups. In the former species two gland cells are constantly anterior 
and four posterior to it; in the latter the distribution is not so regular, as in 
some individuals either two or three cells may compose the anterior set, 
and not infrequently one is also very clearly lateral to the germ cells, 
leaving only two posterior. In both species the coarsely granular proto- 
plasm of these cells readily stains with neutral red in the living animal and 
is eosinophilic in sections (Fig. 16). In C. rhabdocaeca there is a single group 
of six contiguous cells. In C. hamata the penetration gland ducts from the 
two sides run through the center of the body, almost contiguous for the 
greater part of their length; here they are small and difficult to see individ- 
ually. They diverge just behind the pharynx and enter the anterior organ, 
where they expand greatly so that their number and location are more 


315] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 37 


readily determined (Fig. 9). Associated with the gland duct openings is a 
group of about twelve small solid piercing spines which point forward, and 
which are arranged in a crescent around the dorsal side of the mouth open- 
ing. These spines are also solid in C. multicellulata, while in C. rhabdocaeca 
they are hollow. 

The excretory vesicle is a bipartite structure (Fig. 12), the anterior 
part being somewhat larger in all dimensions than the posterior. It is 
about one-fifth as wide as the part of the body in which it is situated. The 
lateral arms branch off without conspicuous enlargement, bend around the 
large germ-cell mass, and continue forward as the main lateral collecting 
tubes. A very small island of Cort is present. The openings of the caudal 
excretory tube branches are in the mid-furcal region. Asin C. multicellulata, 
observation of details is very difficult, and while the locations of all body 
and tail-stem flame cells were made out, the connections of the capillaries 
with the larger tubules have not been determined. The figures for C. multi- 
cellulata serve equally well for the excretory system, except that in C. 
hamata the bending of the main lateral collecting tube is somewhat more 
anterior. In both species this reflexed tube is very clear; it is not shown in 
the figure for C. rhabdocaeca, in which there is no obvious division of the 
main lateral collecting tube into anterior and posterior collecting tubules. 
It is likely that both C. multicellulata and C. hamata possess ciliated areas 
in the main lateral collecting tubes near the entrance of the anterior and 
posterior collecting tubules; several times, at the moment when a cercaria 
was going to pieces due to cover glass pressure, a flickering was noted 
lateral to the anterior cell mass in each species. The flame cells in the tail- 
stem of C. hamata are very small and are seen only with difficulty. 

There are two large cell masses, consisting of a large number of small, 
deeply staining cells, similar in size and location to those of C. multicellulata. 
There are some indications of lateral connections between the two groups 
of cells, and also of lateral extensions forward from the anterior mass which 
meet in a median plane; thus the whole would form a figure eight. Whether 
these are both germ cell masses or the anterior one represents a rudi- 
mentary sucker has not been decided. These conspicuous cell masses were 
not described for C. rhabdocaeca; Faust mentioned a few large germ cells as 
lying ventral to the bladder. 

The parthenitae are long thread-like sporocysts (Fig. 11), not differing 
markedly from those of C. multicellulata. Bright yellow pigment granules 
are seen by reflected light, and examination under higher powers, with 
transmitted light, reveals the presence of other orange-colored spots. 
Waves of contraction, beginning at one end and passing through the entire 
length, were observed in sporocysts taken from the digestive gland soon 
after killing the snail. Puncture of the liver after careful removal of the 
shell results in a very active waving about on the part of protruding sporo- 


ILLINOIS BIOLOGICAL MONOGRAPHS [316 


wn 
~~ 


cysts, even those containing very young germ balls. A birth-pore is present 
(Fig. 14). 

C. hamata was found in one out of sixty specimens of Planorbis trivolvis 
from the drainage ditch, Crystal Lake Park, Urbana, collected September 
25, 1922. On October 26 one P. érivolvis in 101 from the same location was 
infested. On November 4, one-half mile farther up the ditch, a collection 
of eleven of the same species yielded a single infection. 


317] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 59 


CLASSIFICATION 


There are at present upwards of one hundred furcocercous cercariae 
more or less fully described. It does not seem possible to devise a scheme 
of classification, upon either a natural or an artificial basis, which will 
include all forms; it is especially difficult to dispose of those for which only 
external characters are known, since they can not be placed except on the 
basis of general similarities to other completely described cercariae. The 
classification which the author proposes is preceded by a discussion of other 
recent ones. 

The three groups which Cort (1917) established to contain six furcocer- 
cous cercariae were defined in the discussion of his paper in the historical 
section. He studied the homologies of the excretory systems of these larvae, 
and stated that his work had convinced him that ‘‘a more complete know- 
ledge of this system will do much to clear up relationships and to establish 
natural families. Also an increased knowledge of the excretory systems of 
little known types of cercariae will be of great help in solving life-histories 
by suggesting the groups of adults to which such forms belong. In certain 
cases the close relationship of two cercariae may be shown by comparisons 
of their excretory systems, when on account of differing degrees of develop- 
ment of adaptive larval characters they superficially appear to be very 
different.’’ Because only six fully described larvae were available for classi- 
fication, Cort’s scheme is too limited to allow the inclusion of all forms now 
known. 

Sewell’s classification (1922) is the result of a consideration of all well- 
described furcocercous larvae, including the monostomes. Although he 
recognized that these last are more closely related to distome furcocercous 
than to other monostome cercariae, nevertheless he considered them quite 
apart from the distome forms. No pharyngeal monostomes, other than 
those in the peculiar Vivax group, were known at the time of publication 
of his paper; he divided the monostome larvae into the Lophocerca group, 
with furcae shorter than one-half the length of the tail-stem and with a 
mid-dorsal body fin-fold, and the Lophoides group, the single member of 
which has relatively long furcae and no body fin-fold. For the distomes 
Sewell modified Cort’s (1917) grouping to form the basis of his system of 
classification embracing a much larger number of forms. He united the 
first two groups of Cort into Group 1, and divided Cort’s third into two, 
Group 2 and Group 3. Group 1 of Sewell, the brevifurcate apharyngeal 
distomes, was divided into two series mainly on the basis of presence or 


60 ILLINOIS BIOLOGICAL MONOGRAPHS (318 


absence of hollow piercing spines, and of presence or absence of fin-folds 
on the furcal rami; each series was further divided into subgroups, on the 
basis of the complexity of the excretory system pattern. The longifurcate 
distomes, Group 2, were divided into a pharyngeal and an apharyngeal 
series, the latter based on a single new species, C. indica XXII; three sub- 
groups of the pharyngeal larvae were created, chiefly on the basis of the 
excretory system pattern, each to contain a single well-described larva. 
Group 3 was formed to contain C. vivax and two new species of longifurcate 
pharyngeal monostomes having the same peculiar type of excretory system. 
A number of larvae could not be included in his classification, largely be- 
cause of incomplete descriptions. 

Faust (1924) presented a scheme of classification for digenetic trema- 
todes, mostly larvae, in which each ultimate group contains those forms 
whose excretory system formulae may be elaborated from a basic group 
formula. The furcocercous cercariae are placed together in the ninth sub- 
division under Distome Cercariae; furcocercous monostomes are included 
here also. The importance of the excretory system for the establishment 
of natural groups has already been stressed by Cort (1917), and discussed 
in some detail by Faust (1919b, c, d). In the paper now being considered 
Faust places still greater emphasis upon this system; he states (p. 261): 


A study of the larval characters of the trematodes for some years has brought me to the 
conclusion that there is only one common system carried over from the cercaria to the adult, 
which is sufficiently definite and conservative as to be utilizable for purposes of group identifi- 
cation. That system is the excretory system. The more work that is done in this system, the 
more indicative it is of possessing value as a natural basis of classification, and the more 
evident is the artificiality of some of Liihe’s groupings of larval forms and of the equal arti- 
ficiality of some of the families of adult trematodes that have been created. While the study 
of adult correlations with known larval forms is still in its infancy, it is not too much to state 
that all members of a natural adult group possess the same basic excretory pattern. 


This correspondence of close relationship with identical excretory systems 
has already been pointed out for the larvae of the three human schisto- 
somes; furthermore, Faust and Meleney (1924) have shown that the ex- 
cretory system in the post-larval stages of Schistosoma japonicum, the only 
species known in this respect, is a regular elaboration from that system in 
the cercaria. 

Among the furcocercous cercariae about half of the groups had been 
established by Sewell; to some Faust added other larvae, and also set up 
new groups to contain one or more forms. A fundamental formula, with 
possible elaborations worked out a@ priori, was used, and it was found that 
the groups fitted into this formulary scheme, leaving very few gaps. How- 
ever, the present author finds that certain of these groups are not homogen- 
eous. In the Ocellata group are placed C. ocellata, with seven pairs of flame 
cells, arrangement unknown, C. indica XXV with five pairs, C. indica 


319] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 61 


XXXVI with four pairs observed and the possibility of a fifth pair, and 
C. bilharziella, of which nothing is known of the excretory system and 
practically nothing of the general morphology. Furthermore, identical 
formulae are given in two instances for widely separated groups; thus, that 
for the furcicauda group is the same as for the burti group (although in the 
latter it does not include the flame cells in the tail-stem); also the Baiswan 
group in one place, and the emarginatae and tetis groups in another, are 
given identical formulae. This raises the question as to where a new species 
with either of these formulae would be placed; if general structural similar- 
ity is to be taken into account in these instances, it is difficult to see why 
C. douthitti and C. elephantis are placed together, since they are quite dis- 
similar in general organization (Miller, 1924). C. pseudo-vivax nov. sp. and 
C. divaricata nov. sp. were placed in the same group with C. vivax, although 
a complex excretory system of the Vivax type is not described for either. 

Faust states (p. 263) that ‘‘the forms included in this table are by no 
means exhaustive, but no well-described species has been omitted simply 
because it does not fit into the scheme proposed.”’ The present author sees 
no reason why C. indica IX, C. indica XLVII, C. indica LV, C. bombayensis 
no. 8, and C. bombayensis no. 9 were not included. Although in one of these 
species, C. indica XLVI, the exact connections of the flame cell capillaries 
are not shown, the same is true for C. indica XXXVI, which is included in 
the ocellata group. 

The position held throughout as to the significance of the excretory 
system formulae of larvae must be based on the assumption that the elabo- 
ration into the system of the adult will proceed with regular divisions of the 
flame cells of the larva, otherwise the similarities of larval patterns would 
be of less value. The post-larval development has been followed in only one 
species of furcocercous cercariae, the cercaria of Schistosoma japonicum; in 
an early agamodistome stage of this species the posterior flame-cell in the 
body divided and re-established the condition of two flame cells in both 
anterior and posterior groups, thus compensating for the loss of the flame- 
cell in the discarded tail. From this it would seem that some flame-cells of 
the cercaria might have potentialities for more rapid division such that the 
pattern of the adult worm could not be predicted. That this may be the 
case is also indicated by the unequal development in some larvae of the 
anterior and posterior collecting tubule systems, although presumably each 
started with a single flame-cell. Furthermore, the fact that certain larvae, 
including C. robusticauda and C. gigas, have one or more flame-cells con- 
siderably larger than the others may indicate that these cells are about 
ready to divide; but whether they will dichotomize once cr twice in a post- 
larval stage before the other cells do so cannot be predicted. It is extremely 
important that the excretory system pattern be worked out for the early 
post-larval stages of a number of fureocercous cercariae; unhappily only a 


62 ILLINOIS BIOLOGICAL MONOGRAPHS [320 


few life histories are known and so the materials for such studies are 
limited. 

A fact which makes the use of the excretory system not very feasible, 
at least for practical purposes, is the great difficulty with which the pattern 
is determined. Cort, Faust and others have called attention to the tedious- 
ness of the study involved, and their experiences are born out by the studies 
of the present author on more than forty larval species. It is reasonably 
certain that the patterns described for a number of cercariae will have to 
be revised when these species are restudied; a mistake in locating the point 
at which any flame-cell capillary empties into the lateral collecting tubule 
will change the formula. Where the figure does not clearly show the con- 
nections, it may be impossible to decide what formula would represent the 
actual conditions. 

In the scheme to be presented below the presence or absence of a 
pharynx is the first consideration for the division of the furcocercous larvae 
into two main groups; it is held that this character is of more significance 
than the presence or absence of a ventral sucker. This view is supported 
by Stunkard’s (1923) studies on adult blood-inhabiting trematodes from 
reptiles, and his discussion of the relationships of these forms in fishes, 
reptiles, birds and mammals, a discussion in part previously taken up by 
Odhner (1912) and Ward (1921). These studies indicate that the blood 
flukes constitute a natural group. Two of the three families, the Schisto- 
somatidae and the Spirorchidae, include forms which in the older classi- 
fication would have been placed in the widely separate groups of Mono- 
stomes and Distomes. As all of these adults lack muscular pharynges, it 
would seem that the presence or absence of a pharynx is of greatsignificance, 
while the possession or lack of a ventral sucker is relatively unimportant. 
Numerous other studies have shown that the monostomes were probably 
derived from the distomes by a gradual loss of the ventral sucker. Further- 
more, some pharyngeal furcocercous larvae are now known to develop into 
members of the Holostomata, all of which possess pharynges. Accordingly, 
in the classification in this paper a division is first made between the 
pharyngeal and the apharyngeal forms, thus giving much more emphasis 
to this character than Sewell did; each of these groups is then further di- 
vided into brevifurcate and longifurcate larvae; and the monostome and 
distome members of each of the four resulting groups are separately con- 
sidered. 

An attempt has been made to include all furcocercous larvae for which 
there are adequate descriptions. As relatively few are described with 
respect to the exact pattern of the excretory system, all other points of 
morphology have been taken into consideration; even then it has been 
necessary to place many cercariae in a separate list of unclassified forms. 
If Faust’s emphasis on the excretory system as the best criterion for the 


321] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 63 


formation of natural groups were strictly followed, a number of larvae 
would be otherwise allocated in the scheme. To express the degree of de- 
velopment of the excretory system, which is taken into account in the 
formation of the final groups, the formula used by Sewell has been employed 
with a slight modification; for example, the formula for the cercaria of 
Schistosoma japonicum is 2X3(-+1), where two represents the two sides of 
the body, three, the number of flame-cells in one lateral half of the body, 
and, (-++1), the flame cell in one lateral half of the tail. 

By far the greater number of the apharyngeal larvae have furcae which 
are shorter than one-half the tail-stem length; and the opposite is true of 
the pharyngeal forms, in which thirty-eight out of forty-one are longifur- 
cate, with furcae approximately equal to, or in some cases longer than 
the tail-stem. The brevifurcate and longifurcate larvae differ in other 
characters than the relative lengths of furcae and tail-stem, although the 
terms are retained as convenient designations for the groups. They are 


compared below. 


BREVIFURCATE LARVAE 


Furcae usually less than one-half the tail- 
stem length; frequently sharply delimited 
from the tail-stem. 


Tail-stem diameter less than that of body; 
usually attached somewhat ventrally, some- 
times decidedly so, such that a dorso-ventral 
mount is rare. 


Furcal fin-folds sometimes present. 


Body frequently very hyaline. 


Eye-spots may be present. 


Anterior organ a very highly modified oral 
sucker, with anterior thin-walled and pos- 
terior muscular portions; head gland usually 
present. 


Ventral sucker usually much smaller in 
diameter than anterior organ; very protrusi- 
ble and often held protruded. 


Penetration glands very large; frequently 
divided into anterior coarsely granular and 
posterior finely granular cells. 


Penetration gland duct openings frequently 
capped by hollow piercing spines. 


Excretory openings at tips of furcae. Never 
more than one pair of flame cells in proximal 
part of tail-stem. 


Lonorrurcate LARVAE 
Furcae longer than one-half the tail-stem, 


sometimes exceeding it; usually not sharply 
delimited. 


Tail-stem diameter approximately equal to 
that of body when fully extended; attached 
terminally, dorso-ventral mount the usual 
one. 


Furcal fin-folds absent. 


Body usually crowded with small paren- 
chyme cells. 
Eye-spots usually absent. 


Anterior organ less highly modified; cells 
which possibly represent a head gland present 
in but a few larvae. 


Ventral sucker frequently large, in some cases 
of greater diameter than anterior organ. 


Penetration glands small in proportion to 
body; no differentiation into anterior and 
posterior sets. Usually coarsely granular, and 
acidophilic in sections. 

Solid piercing spines more frequent than 
hollow ones. 


Excretory openings typically mid-furcal. 
Usually two pairs of tail-stem flame cells, 
seldom confined to a strictly proximal loca- 
tion. 


64 ILLINOIS BIOLOGICAL MONOGRAPHS 


Tail-stem wall usually provided with power- 
ful longitudinal muscles. Caudal glands not 
conspicuous; when present, are not arranged 
in pairs along caudal excretory tube. 


Tail-stem and furcae usually spined; no 
sensory hairs. Furcae almost cylindrical in 
some larvae. 


Alimentary canal opens more or less ventrally 
as a capillary tube; ceca absent or at most 
very short. 


[322 


Tail-stem wall frequently annulated; tail less 
powerful and more transparent. Conspicu- 
ous, more or less regularly paired caudal 
glands in a number of species. 


Tail-stem usually devoid of spines; furcae 
may be spined; sensory hairs on the tail- 
stems of several larvae. Furcae never cylin- 
drical, usually much flattened. 


Alimentary canal usually opens terminally or 
subterminally; esophagus a fair-sized tube; 
ceca usually well-developed, frequently reach- 


ing almost to posterior end of body. 


APHARYNGEAL CERCARIAE 


It is quite probable that some of the larvae included under this heading 
will be found, upon more careful study, to possess pharynges. Certain few 
larvae have been placed in sub-groups of the pharyngeal forms, in cases 
where other morphological characters strongly justify it, and point to the 
possible incompleteness of the description with respect to the pharynx. 


APHARYNGEAL BREVIFURCATE CERCARIAE 


This group has been most intensively studied, due to the fact that the 
larval forms of the human schistosomes are included here; accordingly the 
data for these cercariae permit the formation of a number of groups, on the 
basis of morphology in general, and in particular the pattern of the ex- 
cretory system. The first division is into distomes and monostomes. These 
two groups are rather sharply divided from each other on the basis of sev- 
eral characters which will be discussed later. 


APHARYNGEAL BREVIFURCATE DISTOME CERCARIAE 
(Sewell’s Group 1) 


Group A (japonicum of Sewell) 
Cercaria of Schistosoma japonicum 
Cercaria of Schistosoma haematobium 
Cercaria of Schistosoma mansoni 
Cercaria indica XXX 
Cercaria in Blacklock and Thompson 1924 


It is now clear that all members of Group A have identical excretory 
system patterns; this consists of three pairs of flame cells in the body and 
one pair in the tail-stem, formula 2X3(+1). It has already been noted that 
the ciliated areas in the excretory vesicle arms were probably mistaken by 
previous workers for flame cells, thus accounting for the larger numbers 


323] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 65 


reported by Miyairi and Suzuki (1914), Ogata (1914) and Iturbe (1917). 
The same perfect agreement is not found in the penetration gland equip- 
ment. The varying number and character of these gland cells in the mem- 
bers of this group have been reviewed in numerous places in the historical 
section, as have also the conflicting statements concerning them within 
what is believed to be a single species. Either the observations have been 
faulty in some cases or there are more species of schistosomes than has 
been suspected. 


Group B (spindale of Sewell, in part) 
Cercaria B of Kemp 
Cercaria of Schistosoma spindale 
Cercaria indica XLVII 


The last two species have four pairs of flame cells in the body and one 
pair in the tail-stem, formula 2X4(+1). The number of penetration glands 
is identical in these two also, namely two anterior pairs with coarsely gran- 
ular protoplasm and three posterior pairs with finely granular protoplasm; 
in C. indica XLVII all five pairs are acidophilic, whereas the three posterior 
pairs of the cercaria of S. spindale are basophilic. Cercaria B is included 
here provisionally, chiefly on the basis of number and character of the 
penetration glands; the excretory system is unknown. This group has not 
been modified from Sewell, except by the addition of Cercaria B. 

Several other forms, which have superficial characters of the schisto- 
somes, but are not sufficiently known to be definitely placed, are included 
here for the sake of completeness. In the single figure given for it, C. 
blanchardi closely resembles the human schistosome larvae; Lutz (1919: 
112) is of the opinion that da Silva studied the cercaria of S. mansoni. The 
cercaria in Leiper (1915, Fig. 46), was considered by him to be a schisto- 
some larva; the figure shows it to have the general characteristics of these 
larvae. The cercaria in Manson-Bahr and Fairley (1920, Pl. III, Fig. 5), 
also seems to belong here; as already noted by Sewell, these authors were 
in error to suppose it to be the same as the form which Leiper provisionally 
called C. bilharziella, which has eye-spots, as these structures appear early 
in development and the figure given by them is of a mature cercaria, 
without eyespots. According to Cawston (1922c), C. crispa is a synonym 
of the cercaria of S. haematobium, and C. spinosa is possibly a synonym 
of the cercaria of S. mansont. 


Group C (douthiiti of Sewell, in part) 
Cercaria douthittr 
Cercaria C of Kemp 
Cercaria of Schistosomatium pathlocopticum 


66 ILLINOIS BIOLOGICAL MONOGRAPHS (324 


This group was created to contain C. douthitti and C. elephantis; these 
two larvae are different in certain respects and have been placed in separate 
groups (Miller, 1924). They differ in character and location of the pene- 
tration gland cells; and almost the entire posterior half of the body of C. 
elephantis is filled with a mass of cells not represented in C. douthitti. 

C. douthitti, the type of the reconstituted group, has the flame-cell 
formula 2X5(-++1). Its close resemblance to the cercaria of Schistosoma- 
tium pathlocopticum, except in the number of penetration gland cells, has 
been pointed out by Tanabe (1923); the excretory systems are identical in 
the number of flame cells. The knowledge of Cercaria C is confined to 
data from preserved material; it belongs here on the basis of general simi- 
larity. 

Groups A, B and C differ chiefly in the complexity of the excretory 
system; the members have from three to five pairs of flame cells in the 
body. Probably all of these larvae will be included in the family Schisto- 
somatidae. 


Group D (elvae) 
Cercaria ocellata 
Cercaria bombayensis no. 19 
Cercaria elvae 
Cercaria gigantea 


The reason for dissolving the Ocellata group of Sewell was stated under 
the description of C. elvae; here also was discussed the similarities of the 
four larvae placed in this group. These forms are especially interesting in 
that they possess many characters of the schistosome cercariae, and yet 
differ in having much more elongate bodies, pigmented eye-spots, and 
possibly furcal fin-folds in C. ocellata; these are the only four brevifurcate 
larvae which do not fall strictly within the definition, but have furcae 
somewhat longer than one-half the tail-stem. Soparkar (1921a) suggested 
that C. bombayensis no. 19 “belongs probably to the ‘Bilharziella’ group of 
cercariae”’; the present author knows of no evidence in support of this 
statement. 


Group E (bombayensis no. 13) 
Cercaria bombayensis no, 13 
Cercaria indica XXV 
Cercaria wardi 


The morphological basis for grouping these forms together was discussed 
in detail under the description of C. wardi. C. bombayensis no. 8, an inter- 
mediate between the apharyngeal brevifurcate monostomes and distomes, 
will be discussed under the group of brevifurcate monostomes; it is some- 
what similar to C. indica XXV. 


325] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 67 


Group F (Wynaad) 
Cercaria indica XXXVI 


Although this larva is in general like the members of Group E, it is here 
tentatively held as the representative of another group; this is partly be- 
cause of the lack of the so-called posterior mucin gland, of unknown func- 
tion and unique to the three members of Group E. Furthermore, it pos- 
sesses a large number of small penetration gland cells, in two differentiated 
sets; and lacks a head gland, found in Group E larvae. 


Group G (elephantis) 
Cercaria elephantis 
ercaria echinocauda 


C. elephantis was placed by Sewell in the Douthitti group, and C. 
echinocauda in the Gigas group. The excretory formula is known for C, 
elephantis only, 2X5(+1). The author studied living material of this 
species, collected from the same region of Michigan as was Cort’s material; 
it was discovered that in addition to the numerous small gland cells which 
distend the posterior part of the body, designated as cephalic glands (Cort, 
1917:53), there are also two distinct sets of penetration gland cells. Five 
pairs are centered around the ventral sucker; three pairs of small cells are 
anterior to two pairs of larger cells. Study of some alcoholic material of 
C. echinocauda (by Miller, 1924) revealed the presence of the same sort ofa 
posterior cell mass as is found in C. elephantis; the number, location and 
relative size of the two sets of penetration glands are also the same. 


Group H (gigas of Sewell, in part) 
Cercaria gigas 


The unique type of excretory system reported for this larva shows that 
it is very different from any other described form. However, it does not 
depart in other of the important characters as far from the Group F or G 
types as might be concluded from Faust’s original description (1918a). The 
author’s material of C. gigas, as well as co-type slides in the collection of 
Professor Ward, shows that an alimentary canal like that described for C. 
wardi is present, contrary to Faust’s statement that pharynx, esophagus 
and ceca are wanting. There are five pairs of large penetration gland cells 
anterior to the germ-cell mass, and two pairs posterior to it. Sewell re- 
garded C. gigas as the highest stage of development in his Group 1, repre- 
senting the culmination of alimentary canal retrogression and excretory 
system development. His conclusion may be justified on the basis of the 
large number of flame-cells; but the larva is not an example of extreme 
degeneration of the alimentary canal. 


68 ILLINOIS BIOLOGICAL MONOGRAPHS [326 


Miscellaneous group 
Cercaria bilharziella 
Cercaria oculata 
Cercaria parvoculata 
Cercaria patialensis 


These larvae complete the list of those known to be apharyngeal brevi- 
furcate distomes. The exact positions of the first three cannot be deter- 
mined until more complete descriptions are available. All four have pig- 
mented eye-spots, and the last three are reported to develop in rediae. C. 
patialensis has a unique excretory system and tail-stem, and has the high- 
est degree of development of the genital system found in the furcocercous 
larvae. It cannot now be placed in relation to any other known form. 

A key for the separation of these sub-groups of the apharyngeal brevi- 
furcate distomes has been published (Miller, 1923). 


APHARYNGEAL BREVIFURCATE MONOSTOME CERCARIAE 


Only two of these forms were known to the earlier workers: C. cristata 
and C. microcristata. To these are to be added C. indica IX, XIII, XXXIX, 
and LV, C. bombayensis no. 8, and the cercaria of Sanguinicola inermis. No 
members have been reported from the fresh waters of this country; one 
unnamed marine species has been described by Linton (1915). As the 
present author has no personal aquaintance with these forms, the attempt 
to critically consider Sewell’s disposition of them will be based entirely on 
a study of the literature. His analysis took into account all species except 
the cercaria of Sanguinicola inermis, and incorrectly included C. varicans, 
which is clearly figured by Abildgaard as a longifurcate larva, with furcae 
almost if not quite as long as the tail-stem. Sewell took the group name 
Lophocerca from Lihe; the most striking features of these larvae are the 
presence of a body crest and the absence of any trace of pharynx or in- 
testine. The group can not be subdivided, as Sewell’s species are the only 
ones for which the excretory and penetration gland systems are known. 

The original account of C. cristata has been studied, as have also the 
numerous subsequent references to it by other workers; it seems probable, 
as Sewell suggested, that more than one larva has been included under this 
specific name. Because of its inadequate description Scheuring concluded 
that the identity of this species with the cercaria of Sanguinicola inermis 
was doubtful. Ercolani described C. microcristata as similar to C. cristata 
except for smaller size. Both C. bombayensis no. 8 and the cercaria of 
Sanguinicola inermis have been described in sufficient detail so that they 
could readily be recognized. As Sewell noted, the former of these two is 
intermediate between the monostomes and distomes, both in the presence 
of a small body crest and of a group of cells probably representing a rudi- 


327] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER_ 69 


mentary ventral sucker. The descriptions of the four new Indian species 
contribute many details of structure not previously known for brevifurcate 
monostomes; Sewell believes that C. indica XIII is only questionably 
distinct from C. cristata. 


Lophocerca Group of Sewell, in part 
Cercaria cristata 
Cercaria microcristata 
Cercaria of Sanguinicola inermis 
Cercaria bombayensis no. 8 
Cercaria indica IX 
Cercaria indica XIII 
Cercarta indica XXXIX 
Cercaria indica LV 


Here are briefly recapitulated some of the characters enumerated by 
Sewell: the body is provided with a dorsal longitudinal crest; a definite oral 
sucker is absent, and the anterior end forms a conical protrusible and re- 
tractile snout; there is no trace of pharynx or intestine; where the excretory 
system has been worked out, the formula is 2X3(-++0); development is in 
small rounded or oval sporocysts. It is to be noted that there are no flame- 
cells in the tail-stem of these larvae, which makes them unique among 
furcocercous forms. 


APHARYNGEAL LONGIFURCATE CERCARIAE 


In general these larvae resemble the pharyngeal longifurcates more 
closely than other apharyngeal larvae, either distomes or monostomes. 
Nevertheless, it is thought that the presence or absence of a pharynx is of 
more significance than similarity in larval characters. The few cercariae 
under this heading are not all well-described; they do not seem to form a 
homogeneous group, and the disposition of them into sub-groups will have 
to be postponed until more species are described. 


Apharyngeal Longifurcate Distome Cercariae 
Cercaria gracillima 
Cercarta tubertstoma 
Cercaria gladii 
Cercaria minima 
Cercaria indica XXII 
Cercaria in Lagrange 1923:175 


Apharyngeal Longifurcate Monostome Cercariae 
Cercaria indica XXVII 


70 ILLINOIS BIOLOGICAL MONOGRAPHS [328 


This is the only unquestionable representative of this group. Repeated 
studies on C. muilticellulata failed to show any trace of a pharynx, but ob- 
servation was hindered by the numerous refractile parenchyme cells crowd- 
ing the body; and this larva is so strikingly similar in most respects to C. 
hamata, which has a definite pharynx, that it has been classed with the 
pharyngeal forms. C. indica XXVII is not very similar to any of the six 
apharyngeal longifurcate distomes, from which group it would presum- 
ably have been derived by loss of the ventral sucker. Its resemblance to 
the schistosomes in two characters was pointed out by Sewell, that is, the 
presence of an anterior protrusible penetrating organ and an exactly similar 
excretory system. 


PHARYNGEAL CERCARIAE 


Approximately one-half of the furcocercous cercariae are known to 
possess pharyngeal sphincters. The first division of these, as with the 
apharyngeal cercariae, is made between the longifurcate forms, of which 
there are thirty-eight, and the three brevifurcate forms. 


PHARYNGEAL BREVIFURCATE CERCARIAE 


Pharyngeal Brevifurcate Distome Cercariae 
Cercaria scripta 
Cercaria parthenicola 
Cercaria octadena 


Until more complete accounts of these forms are available, including 
analyses of the excretory system patterns in living material, little can be 
said of their relationships; the first two were reported to develop in rediae. 
It is surprising that Faust believes C. octadena to be the larva of Schisto- 
soma bovis; he figured it with a small pharynx. This is the only recent 
account which assigns a pharyngeal larva to the family Schistosomatidae. 


Pharyngeal Brevifurcate Monostome Cercariae 
No representatives 


PHARYNGEAL LONGIFURCATE CERCARIAE 


This is the largest group of furcocercous larvae, and the one concerning 
the adult affinities of which nothing was known until the work of Ruszkow- 
ski, Lutz, and Szidat. Many of the members are very incompletely de- 
scribed, and relatively few are known with respect to the excretory system 
pattern. This system was not described in the cercaria of Hemistomum 
alatum; it was only partially figured by Szidat in Cercaria A, which develops 
into Tetracotyle typica. Hence other cercariae for which the complete ex- 
cretory patterns are known cannot be placed in relation to these known 
holostome larvae. 


329] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 71 


PHARYNGEAL LONGIFURCATE DISTOME CERCARIAE 
(Sewell’s Group 2, Series 1) 


In his consideration of these forms Sewell created three sub-groups, each 
to contain a single cercaria; five other incompletely described larvae were 
referred either tentatively to one of these sub-groups, or to the series. At 
the present time there are thirty-one of these cercariae, and probably other 
members which are classed among the partially known and unplaced forms. 
The penetration glands have been described in twenty-one larvae, and the 
entire excretory system is known for eleven species, with incomplete de- 
scriptions for five more. Only sixteen larvae have been described with 
respect to both systems. In spite of this great increase over the number 
considered by Sewell, the present author has not been able to establish a 
satisfactory scheme of relationships, due to the paucity of morphological 
data. The great diversity, even in the eleven fully described species, of 
flame cell number and of nature and number of the penetration glands 
makes it almost impossible to arrange them in any feasible systematic 
scheme. The author has been unable to find correlation between any two 
of the following: body, tail-stem and furcal lengths; number and arrange- 
ment of flame cells; number, location in body, and character of penetration 
gland cells; type of alimentary canal; size and location of ventral sucker. 

The following belong here; formulae for the excretory system are in- 
cluded. 

Cercaria A (Szidat) 


aculeata 
“  B (Szidat) 
‘“  bdellocystis 
“  bombayensis no. 9 2 10(+2) 
“  burti 2X 6(+2) 
“ C (Szidat) 
“«  chrysenterica 2X7(+2) 
“  divaricata 
«  douglasi 2X5(+2) 
“€  emarginatae 2X5(+2) 
“  fissicauda 
“ furcicauda 2X5(+1) 
© gracilis 
“ gyrinipeta 
Cercaria of Hemistomum alatum 
‘in Hesse 1923 2X7(+2) 
Cercaria indica I 2X5(+1) 


«indica II 2 10(+2) 


72 ILLINOIS BIOLOGICAL MONOGRAPHS [330 


“  letifera 

«  longissima 
Cercaria in Manson-Bahr and Fairley (1920, Pl. III, Fig. 7) 
Cercaria minuta 

“  molluscipeta 
pseudo-vivax 
“*  quattuor-solenata 2X6(+2) 
redicola 
“  robusticauda 2X6(+1) 
secobit 
“tenuis 2X5(+2) 


PHARYNGEAL LONGIFURCATE MONOSTOME CERCARIAE 


These larvae fall into two closely circumscribed groups. The first is 
the one which Sewell set up to contain C. vivax and two new species which 
he described. All members have a unique type of excretory system in the 
body, and three pairs of flame-cells in the tail-stem; in no case do the num- 
erous penetration gland cells extend into the posterior half of the body. 
Only one larva, C. leptoderma, is to be added to this group; neither C. 
pseudo-vivax nor the cercaria in Leiper and Atkinson 1915 have been shown 
to have the highly developed excretory system, although Faust has in- 
cluded the former in the Vivax group. C. indica XXXIII (tetis group of 
Sewell) has the same unique arrangement of collecting tubules in the body, 
but only five pairs of flame-cells in the body and two pairs in the tail-stem; 
it probably is the sole known representative of a sub-group. Although C. 
vivax possesses a ventral sucker, this structure is either entirely lacking or 
represented by a mass of cells in the other members. It would seem that 
the very unique development of the excretory system, together with the 
three pairs of flame-cells in the tail-stem, is of more significance than the 
presence or absence of a ventral sucker. 


Vivax group (Sewell’s Group 3) 
Cercaria vivax 
Cercaria indica XV 
Cercaria indica LVIII 
Cercaria leptoderma 


Tetis group of Sewell 
Cercaria indica XXXIII 


The remaining group contains C. rhabdocaeca, C. hamata, and C. multi- 
cellulata. As noted above, a pharynx was not observed in the last-men- 
tioned larva. It is included here because of many striking similarities, 
which have been discussed under the description of C. hamata. All three 


331] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 73 


species have eight pairs of flame cells in the body and two pairs in the tail- 
stem. 


Rhabdocaeca group 
Cercaria rhabdocaeca 
Cercaria hamata 
Cercaria multicellulata 


FURCOCERCOUS CERCARIAE OF UNCERTAIN POSITION 


The following forms have been incompletely described with respect to 
the presence of a pharynx, the character of the excretory system, or the 
penetration glands. In some cases, as where a microphotograph is given 
without description in the text, it is not clear whether a ventral sucker is 
present. The probable groupings of all are given, on the basis of all known 
characters. 

Brevifurcate Distomes 

Cercaria andot 

Cercaria in Lagrange (1923:177); probably apharyngeal 

Cercaria in Manson-Bahr and Fairley (1920, Pl. III, Fig. 5); proba- 
bly apharyngeal 


Brevifurcate Monostomes 
Cercaria senoi 
Cercaria in Lithe (1909:206) 


Longifurcate Distomes 
Cercaria furcata 
“  ainversa 
Cercaria in Liithe (1909:204) 
_ in Leiper and Atkinson (1915) 
Cercaria paludinarum 
“  pseudo-divaricata 
quieta 
shinchikuensis 
“  valdefissa 


Longifurcate Monostomes 
Cercaria varicans 


Unknown 
Cercaria bipartita 
Cercaria in Lagrange (1919) 
Cercaria ocellifera; brevifurcate, probably apharyngeal 


ILLINOIS BIOLOGICAL MONOGRAPHS {332 


CHECK-LIST OF FURCOCERCOUS CERCARIAE 


The following list contains the specific names and references to the 
original descriptions of all furcocercous cercariae, both fresh-water and 
marine; the latter, included for the sake of completeness, are separately 
grouped at the end. The synonyms and descriptive modifications of Cer- 
caria are also given. In cases where the original descriptions are very brief 
or entirely inadequate, and a later study has been comprehensive, this 
latter reference is also given. 


FRESH WATER SPECIES 


Cercaria A in Kobayashi 1922:14, for Cercaria of Seno 1903; renamed C. senoi in Faust 


1924:296 

A in Szidat 1924:301-303; text-fig. 1 

aculeata in Ercolani 1882:47; Pl. 1, figs. 42-46 

sp. [X in Ando 1918:616; renamed Cercaria C in Kobayashi 1922:14; renamed C. 
pseudodivaricata in Faust 1924:296 

sp. X in Ando 1918:617; renamed Cercaria B in Kobayashi 1922:14; renamed 
C. andoi in Faust 1924:296 

andoi in Faust 1924:296, for Cercaria sp. X in Ando 1918:617 and Cercaria B in 
Kobayashi 1922:14 

B in Kemp 1921:231-232; text-fig. 1, d, ¢ 

B in Kobayashi 1922:14, for Cercaria sp. X in Ando 1918:617; renamed C. andoi 
in Faust 1924:296 

B in Szidat 1924:303; text-fig. 2 

VI in von Baer 1827:627; Pl. 31, figs. 6a, 6b; synonym of Malleolus furcatus in 
Diesing 1850:295; synonym of C. furcata in Moulinié 1856:168 

bdellocystis on page 77, for Dicranocercaria bdellocystis in Lutz 1921:126 
bilharziella in Leiper 1915:259 

bilharziellalunata nom. nud., synonym of C, oculata according to Faust 1920b:216 
bipartita in Sonsino 1897:253 

in Blacklock and Thompson 1924:212-220; 3 text-figs. 

blanchardi in da Silva 1912:398-400; 3 ‘figs. 

bombayensis no. 8 in Soparkar 1921a:24-26; Pl. III, 4 figs. 

bombayensis no. 9 in Soparkar 1921a:26-28; Pl. IV, 4 figs. 

bombayensis no. 13 in Soparkar 1921a:29-30; Pl. V, 4 figs. 

bombayensis no. 19 in Soparkar 1921a:30-32; Pl. VI, 3 figs. 

burti in Miller 1923; in the present paper, page 41 

C in Kemp 1921:232; text-fig. 1, f 

C in Kobayashi 1922:14, for Cercaria sp. [IX in Ando 1918:616; renamed C. pseudo- 
divaricata in Faust 1924:296 

C in Szidat 1924:303-304; text-figs. 3a, 3b 

chrysenterica in Miller 1923; in the present paper, page 47 

crispa in Cawston 1920a:439, synonym of the cercaria of Schistosoma haematobium 
according to Cawston 1922c:247 

cristata in LaValette St. George 1855:23; Pl. Il, K 


333] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER= 75 


“ 


“ 


D in Kobayashi 1922:15, for Cercaria sp. XIV in Nakagawa 1915:116; renamed 
C. paludinarum in Faust 1924:296 
divaricata in Faust 1924:256; Pl. II, fig. 12 
divaricauda in Faust 1924:283; Table I, page 296; Table I, opp. page 298; error for 
C. divaricata 
douglast in Cort 1917:53-54; text-fig. 2, C 
douthittt in Cort 1914:77-78; text-fig. 10; 1915:49-52; Pl. VII, figs. 55-64 
E in Kobayashi 1922:15, for Cercaria sp. XV in Nakagawa 1915:116; renamed C. 
shinchikuensis in Faust 1924:296 
echinocauda in O’Roke 1917:170-171; Pl. V, figs. 39-45; according to Miller 1924: 
146-148; Pl. VI, figs. 4, 6 
elephantis in Cort 1917:52-53 
elvae in Miller 1923; in the present paper, page 30 
emarginatae in Cort 1917:53; text-fig. 2, B 
F in Kobayashi 1918:61; text-figs. 11, 12; 1922:15; Pl. IV, figs. 1, 2; renamed 
C. parthenicola in Faust 1924:296 
jissicauda in La Valette St. George 1855:21; Pl. II, figs. VI and H 
furcata in Nitzsch 1817:49; Pl. 2, figs. 12-18 
furcicauda in Faust 1919¢:336-337; text-fig. 6 
G in Yoshida 1917:117; Pl. II, figs. 17, 18, text-fig. 11; in Kobayashi 1922:16; 
renamed C. scripta in Faust 1924:296 
gigantea in Faust 1924:257; Pl. II, fig. 13 
gigas in Faust 1918a:105-107; Pl. II, figs. 25-30 
gladiit in Cawston 1918a:96; according to Faust 1919a:164-165; Pl. XVIII, fig. 1 
gracilis in La Valette St. George 1855:20; Pl. I, fig. XIII 
gracillima in Faust 1917:122; Faust 1918:80; figs. 142-154, 161 
gyrinipeta in the present paper, page 77, for Dicranocercaria gyrinipeta in Lutz 
1921:126 
H in Kobayashi 1922:16, for the cercaria of Schistosoma japonicum in Miyairi and 
Suzuki 1914 
hamata in Miller 1923; in the present paper, page 55 
of Hemistomum alatum in Ruszkowski 1922:237-250; 3 text-figs. 
in Hesse 1923:227-231; 8 text-figs. 
I in Kobayashi 1922:17, for Cercaria sp? in Suzuki and Nishio 1914; renamed C. 
longissima in Faust 1924:297 
oe I in Sewell 1922:268-270; Pl. XXIX, figs. 1, 2 
II in Sewell 1922:271-274; Pl. XXIX, figs. 3, 4 
IX in Sewell 1922:47-50; Pl. IV, figs. 1, 3 
XIII in Sewell 1922:50-53; Pl. IV, figs. 3, 4 
XV in Sewell 1922:280-288; Pl. XX XI, figs. 1, 2 
XXII in Sewell 1922:276-278; Pl. XXX, figs. 1, 3 
XXV in Sewell 1922:260-262; Pl. XXVIII, figs. 1-3 
XXVIII in Sewell 1922:59-61; Pl. V, fig. 3 
XXX in Sewell 1919:425; Pl. XXV; 1922:251-254; Pl. XXVII, figs. 1-3 
XXXII in Sewell 1922:292-294; Pl. XXX, figs. 4, 5 
XXXVI in Sewell 1922:263-265; Pl. XXVIII, figs. 4, 5 
XXXIX in Sewell 1922:53-55; Pl. V, fig. 1 
“XLVI in Sewell 1922:255-257; Pl. XXVII, figs. 4, 5 
“ LV in Sewell 1922:55-57; Pl. V, fig. 2 
“~ LVITI in Sewell 1922:290-291; Pl. XXXI, fig. 3 
inversa in O’Roke 1917:169-170; Pl. V. figs. 46-51 
J in Kobayashi 1922:17; Pl. IV, figs. 3-5; renamed C. redicola in Faust 1924:297 


2-27 R: ok Re ce UR, Ce ae 


76 


ILLINOIS BIOLOGICAL MONOGRAPHS [334 


sp. no. 1 in Lagrange 1919:386 

in Lagrange 1923:175 

in Lagrange 1923:177 

in Leiper 1915, text-fig. 46; 1918:239, 241 

in Leiper and Atkinson 1915:202; fig. 6 

leptoderma in Faust 1922a:255-257; Pl. XXI, figs. 7-11 

letifera in Fuhrmann 1916:389-393; Pl. I, figs. 1-8, 10 

longissima in Faust 1924:297, for Cercaria sp? in Suzuki and Nishio 1914 and 
Cercaria I in Kobayashi 1922:17 

in Liihe 1909:204 

in Liihe 1909:206 

in Manson-Bahr and Fairley 1920:54; PJ. III, fig. 5 

in Manson-Bahr and Fairley 1920:54; Pl. III, fig. 7 

marcianae in LaRue 1917:3; Pl. I, figs. 1, 2; synonym of A gamodistomum marcianae 
in Cort 1918a:130 

microcristata in Ercolani 1881:56-57; Pl. I, figs. 23-27 

minima in Faust 1919:92, for C. minor Faust 1918a, preoccupied by Lebour 1912:424 
minor in Faust 1918a:107-109; Pl. II, figs. 31-33; synonym of C. minima in Faust 
1919:92 

minuta in Ercolani 1882:46-47; Pl. I, figs. 1-6 

molluscipeta in the present paper, page 77, for Dicranocercaria molluscipeta in Lutz 
1921:126 

multicellulata in Miller 1923; in the present paper, page 50 

sp. XIV in Nakagawa 1915:116; fig. 14; renamed Cercaria D in Kobayashi 1922:15; 
renamed C. paludinarum in Faust 1924:296 

sp. XV in Nakagawa 1915:116; fig. 15; renamed Cercaria FE. in Kobayashi 1922:15; 
renamed C. shinchikuensis in Faust 1924:296 

ocellata in LaValette St. George 1855:22; Pl. II, fig. V 

ocellifera in the present paper, page 73, for Dicranocercaria ocellifera in Lutz 1919: 
Pl. 41, figs. 64-66 

octadena in Faust 1921d:11-12; Pl. III, fig. 1 

oculata in Cawston 1917:132 

paludinarum in Faust 1924:296, for Cercaria sp. XIV in Nakagawa 1915:116, and 
Cercaria D in Kobayashi 1918:15 

parthenicola in Faust 1924:296, for Cercaria F in Kobayashi 1918:61 

parvoculata in Cawston 1919a:401, according to Faust 1919a:165; Pl. XVIII, fig. 2 
patialensis in Soparkar 1924:933-941; Pl. LXII, figs. 1-12 

pseudo-divaricata in Faust 1924:296, for Cercaria sp. IX in Ando 1918:616, and 
Cercaria C in Kobayashi 1922:14 

pseudo-vivax in Faust 1924:255; Pl. II, fig. 11 

quattuor-solenata in Faust 1919c:337-338; text-fig. 8 

guieta in O’Roke 1917:171-172; Pl. IV, figs. 32, 33, 37 

redicola in Faust 1924:297, for Cercaria J in Kobayashi 1922:17 

rhabdocaeca in Faust 1919c:338-339; text-fig. 9 

robusticauda in Faust 1919c:337; text-fig. 7 

of Sanguinicola inermis in Scheuring 1920:227; 1 text-fig.; Scheuring 1922:296-299; 
Pl. 23; fig. 12; text-fig. C 

of Schistosoma haematobium in Leiper 1915:258; text-fig. 47; according to Faust 
1920a:192-193; Pl, XV, figs. 1, 3; according to Bettencourt and da Silva 1922:1050; 
1 text-fig. 

of Schistosoma japonicum in Miyairi and Suzuki 1914:187-197; 1 fig.; according to 
Cort 1919:485-507; text-figs. 1-3 


335] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 77 


Cercaria 


of Schistosoma mansoni in Leiper 1915:258; text-fig. 45; according to Faust 1920a: 
192-193; Pi. XV, figs. 2, 5, 6; according to Khalil 1922: 27-34; text-figs. 1, 2 

of Schistosoma spindale in Soparkar 1921:1-22; Pl. I, II 

of Schistosomatium pathlocopticum in Tanabe 1923:183-186; Pl. XIV 

scripta in Faust 1924:296, for Cercaria G in Yoshida 1917:117, and Cercaria G in 
Kobayashi 1922:16 

secobiana in Cawston 1917:133; synonym of C. secobii in Cawston 1917b:91 

secobit in Cawston 1915:1427; according to Faust 1921d:12; Pl. III, fig. 2 

in Seno 1903:309; Pl. VII, figs. 2A, B; named Cercaria A in Kobayashi 1922:14; 
renamed C. senoi in Faust 1924:296 

senoi in Faust 1924:296, for the cercaria in Seno 1903:309, and Cercaria A in Ko- 
bayashi 1922:14 

shinchikuensis in Faust 1924:296, for Cercaria sp. XV in Nakagawa1915:116 and 
Cercaria E in Kobayashi 1918:15 

spinosa in Cawston 1919:189, synonym of the cercaria of Schistosoma mansoni (?) 
in Cawston 1922c:247 

in Suzuki and Nishio 1914:587; 3 figs; named Cercaria Tin Kobayashi 1922:17, 
renamed C. longissima in Faust 1924:297 

tenuis in Miller 1923; in the present paper, page 45 

tuberistoma in Faust 1917:123; 1918:82-83; Pl. LX, figs. 155-158 

valdefissa in the present paper, page 77, for Dicranocercaria valdefissa in Lutz 
1919:Pl. 41, figs. 67, 68 

varicans in Abildgaard 1794:89; Pl. Ila, figs. 1-4 

vivax in Sonsino 1892:137; Pl. XVIII, fig. 3; according to Looss 1896:210-223; 
Pl. XV, figs. 162-177 

wardi in Miller, 1923; in the present paper, page 35 


MARINE SPECIES 


dichotoma in Miiller 1850; according to La Valette St. George 1855: Tab. II, fig. 1 
discursata in Ssinitzin 1911:67; figs. 45-48 

of Haplocladus minor? in Odhner 1911b:105 

in Haswell 1902:497-511; Pls. 19, 20, figs. 1-31 

in Linton 1915:115-118; text-figs. 1-5 

in Linton 1915a:207-208; text-figs. 7, 8 

in Morgan 1891:1137-1139; 1 text-fig. 

syndosymae in Pelseneer 1906; 172; Pl. IX, X, figs. 20-22 


SYNONYMS 


C. (Schizocerca) dichotoma in Diesing 1858:265; synonym of Cercaria dichotoma 
C. (Schizocerca) fissicauda in Diesing 1858:265; synonym of Cercaria fissicauda 
C. (Schizocerca) gracilis in Diesing 1858:264; synonym of Cercaria gracilis 
Cheilostomum varicans in Diesing 1850:293; synonym of Cercaria varicans 
Dicranocercaria bdellocystis in Lutz 1921:126; synonym of Cercaria bdellocystis 
Dicranocercaria gyrinipeta in Lutz 1921:126; synonym of Cercaria gyrinipeta 
Dicranocercaria molluscipeta in Lutz 1921:126; synonym of Cercaria molluscipeta 
Dicranocercaria ocellifera in Lutz 1919:Pl. 41; synonym of Cercaria ocellifera 
Dicranocercaria valdefissa in Lutz 1919:Pl. 41; synonym of Cercaria valdefissa 
Histrionellina fissicauda in Diesing 1858:269; synonym of Cercaria ocellata 
Lophocercaria fissicauda in Diesing 1858:243; synonym of Cercaria cristata 
Malleolus furcatus in Ehrenberg 1838:465; synonym of Cercaria furcaia 
Schistocercaria, proposed by Soparkar, 1921, for cercariae known to be the larval stages 
of schistosomes. 


78 ILLINOIS BIOLOGICAL MONOGRAPHS [336 


DISCUSSION OF LIFE HISTORIES 


Although brief references to the life history studies on furcocercous 
cercariae are included in the historical review, they are brought together 
here in order to sum up the present knowledge of the group in this field. 
Until recently the three species of human schistosome cercariae were prac- 
tically the only larvae for which the adults were known. Schistosoma japon- 
icum was the first which was shown to have as its larval stage a furcocer- 
cous cercaria (Miyairi and Suzuki, 1913, 1914). Leiper (1915) subsequently 
proved that both of the other human schistosomes, S. haematobium and 
S. mansoni, also developed directly from such larvae found in certain of 
the molluscs of Egypt. These findings exploded the theory Looss held 
persistently for so long, that adult schistosomes developed directly from 
miracidia without the intervention of an intermediate mollusc host. The 
life history of another of these forms, S. spindale, parasitic in cattle in India, 
has been experimentally demonstrated (Liston and Soparkar, 1918). Very 
recently the life cycle of a North American trematode, Schistosomatium 
pathlocopticum, a new genus and species of the family Schistosomatidae, 
has been worked out (Tanabe, 1923). The larva is a brevifurcate distome 
very similar to Cercaria douthitti; it has been experimentally shown to 
develop in laboratory rats. Thus five furcocercous cercariae, all brevifur- 
cate distomes, are known to develop into members of the family Schisto- 
somatidae, following direct penetration of epithelial surfaces of the final 
host. 

Previous to this no complete life histories were known; brief notes on a 
few forms appear in the literature before 1913. In the case of C. fissicauda 
there is an indication of one stage in the life history. Blochmann (1910) 
noted that this cercaria penetrated and caused the death of several species 
of fish and of axolotyl and salamander larvae, being found in large numbers 
in the freshly-examined brain, heart and heart blood. Experiments ap- 
parently were not carried on to determine whether the cercariae would 
develop further in any of these animals. Some unpublished observations of 
Looss on the life history of Sanguinicola inermis were included by Odhner 
(1911) as an addendum to his discussion of this trematode. Goldfish and 
carp in aquaria with Lymnaea auricularia harboring a furcocercous cercaria 
became infested in every case with large numbers of young worms, which 
were found in the mouth cavity and on the gills. In the carp only, these 
became sexually mature in the blood stream. Only one figure, without an 
accompaning description, was given for the larva, which is clearly a brevi- 
furcate monostome; although Looss called it C. cristava. the information 


337] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 79 


given is not sufficient to establish its identity with this species. Scheuring 
has raised this question. The adult worms found were Sanguinicola inermis. 
In a parallel case to that of C. fissicauda above, C. letifera caused the death 
of five species of fish kept in small aquaria with the mollusc host (Fuhr- 
mann, 1916); death was said to be due to hemorrhages and capillary 
obstruction caused by migrations of the larvae. Without further experi- 
mental proof, Fuhrmann supposed the intermediate host to be one or 
several species of fish, and the definitive host to be probably a piscivorous 
fish or bird. 

The agamodistome stages of two cercariae were found in Thamnophis 
marciana and T. eques by LaRue (1917), who called them Cercaria mar- 
cianae and C. vergrandis. The first, more properly called Agamodistomum 
marcianae, was studied by Cort (1918); on the basis of its excretory and 
penetration gland systems he concluded that it is the agamodistome stage of 
a furcocercous cercaria, similar to but not identical with either C. emar- 
ginatae or C. douglasi. 

The life history of Sanguinicola inermis has been experimentally worked 
out in detail by Scheuring (1920, 1922); although the larval form is very 
similar to C. cristata, Scheuring concluded that the identity of the two 
forms is doubtful. The larva reaches the blood stream of its final host, a 
fish, by direct penetration. The relationship of Sanguinicola, family Aporo- 
cotylidae, to the Spirorchidae and Schistosomatidae has been reviewed in 
the historical section of the present paper. 

Several furcocercous cercariae from Brazil have been traced through all 
stages to tetracotyles, after penetration of an intermediate host; and these, 
when the proper final host was found by experimental feedings, developed 
into members of the genus Strigea (Lutz, 1921). In the cases of three new 
species, Cercaria molluscipeta, C. gyrinipeta, and C. bdellocystis, the first- 
named penetrated and continued development in snails, the second in 
tadpoles, and the third in leeches. One of the most interesting discoveries 
was that these cercariae do not immediately encyst in the tissues of the 
intermediate host, but pass a longer precystic stage free in the tissues, 
during which important structural modifications are undergone. The de- 
velopment of the genital system and the definitive form of the body does 
not take place until transfer into the final host. 

The life history of an European member of the Holostomata Hemisto- 
mum alatum, has been experimentally determined by Ruszkowski (1922); 
he cultured the eggs and attempted to infest snails. The miracidia de- 
veloped in several species of Planorbis, and elongate sporocysts and longi- 
furcate distome cercariae were secured. The description of the latter is not 
sufficiently detailed to enable them to be placed in a classification scheme. 
Although the life cycle from cercaria to adult worm has not yet been traced, 
Ruszkowski’s findings supplement those of Lutz on holostomid develop- 


80 ILLINOIS BIOLOGICAL MONOGRAPHS [338 


ment. It is now clear that the Holostomata develop from cercariae which 
have their origin in parthenitae in snails; these, so far as is known, are 
pharyngeal longifurcate distomes. The mode of development of this group, 
so long unknown, has now been experimentally determined. 

Cercaria vivax may penetrate the skin and perhaps the digestive tube 
of certain tadpoles so rapidly, under experimental conditions, as to cause 
death in fifteen minutes (Brumpt, 1922); while the development was not 
followed out, it was thought that it is the larva of a member of the Holosto- 
mata, closely allied to the genus Tylodelphis. The development of another 
larva, resembling C. fissicauda, was followed in tadpoles; this form does 
not encyst and is said to be a larva of the genus Tylodelphis. 

A pharyngeal longifurcate distome cercaria, designated Cercaria A, was 
found by Szidat (1924) to develop into Tetracotyle typica in Lymnaea palus- 
tris. Penetration of the snail host takes place very rapidly, usually in 
fifteen to twenty seconds, and the larvae rapidly make their way directly 
to the hermaphrodite gland. There a more or less complete structural re- 
organization takes place, and only relatively late in development is a cyst 
secreted. The entire development from cercaria to tetracotyle requires 
from twenty to twenty-five days; earlier workers have shown that Teira- 
cotyle typica develops to a species of Strigea, probably S. tarda. 

From this survey of the literature it is clear that much light has recently 
been thrown on the kinship of furcocercous cercariae to certain groups of 
adult trematodes. The larvae of the Schistosomatidae, and of some, pos- 
sibly all, of the Holostomata are included among them. Sanguinicola 
inermis of the Aporocotylidae also has a furcocercous larva. 


339] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 81 


INCIDENCE OF INFECTION OF SNAILS 


Collections were made through three years, and the method of handling 
them changed during this time. At first snails were dissected almost im- 
mediately after collection, and only furcocercous infections were recorded; 
percentages therefore include both mature and immature larvae. During 
the summer of 1921 the method of isolating to secure emerging cercariae was 
begun; only mature larvae were found, as the negative snails were not later 
dissected. However, both furcocercous and other forms were recorded. 
During 1922-23 a complete infection record was kept, including both fur- 
cocercous and other infections, emerging larvae and those found by sub- 
sequent dissection of the snails. 


MULTIPLE INFECTIONS 


As the matter of multiple infections is of some biological interest, the 
cases found (double infections) are grouped together here. 

1. Planorbis trivolvis (March 2, 1921) infested with C. echinocauda anda 
redia resembling that of C. inhabilis. 

2. Planorbis trivolvis (March 16, 1921) infested with an unidentified 
immature furcocercous cercaria and a redia resembling that of C. inhabilis. 

3. Physa lordi (July 8, 1921) infested with an unidentified immature 
furcocercous larva and the cercaria of Echinostomum revolutum? 

The third was a single individual given to the author, and so does not 
appear in the collection records. As all snails were not dissected, it is 
possible that there were other multiple infections which were not found. 


TABLE [+ 


Collection record for 1920-1921; vicinity of Urbana, Illinois. 
All snails were crushed; therefore percentages include both mature and immature in- 
fections (furcocercous cercariae only). 


Species of snail Place Date Number Infections Percentages 
Planorbis trivolvis........ Cc Oct. 12 53 1 (C. elephantis) 1.9 
PHYSG, BYTING ou od eds vas C- .Oct.12 17 0 0 
Campeloma rufum....... Hi- - ‘Oct. 30 51 0 0 
Planorbis trivolvis........ D~ Oct. 30 7 0 0 
Planorbis trivolvis........ D_ Nov. 27 11 0 0 
Planorbis trivolvis........ C Feb. 16 37 1 (C. echinocauda) 237 
PRYSC.BYTING) ico me cid ota an CC Feb. 16 15 0) 0 
Planorbis trivolvis........ C Mar. 2 58 1(Double infection No. 1) 137 
Planorbis trivolvis........ C Mar. 16 15 1 (Immature Cercaria sp.) 


1 (Double infection No. 2) 13.3 


82 ILLINOIS BIOLOGICAL MONOGRAPHS [340 


Physa gyrina............ C Mar. 16 10 0 0 
Planorbis trivolvis........ C Mar. 25 18 1 (Immature Cercaria sp.) 5.5 
Physa gyrina............ C Mar. 25 1 0 0 
Planorbis trivolvis........ C Apr. 6 13 1 (C. wardi) 7.7 
Planorbis trivolvis........ C Apr. 7 37 2 (Cercaria sp.) 

1 (C. wardi) 8.1 
Planorbis trivolvis........ C Apr. 19 29 1 (C. ward) 3.4 
Physa gyrina............ _C Apr. 19 12 0 0 


C, Colvin’s Field; D, Drainage Ditch; H, Homer Park. 


TABLE IT 


Collection record, summer of 1921; vicinity of Douglas Lake, Michigan. 
Snails were isolated for emerging cercariae and were not later crushed; therefore immature 
infections were not found. 


Infections Furco- 
Species of snail Place Date Number other than Furcocercous cercous 
furcocercous infections percentage 
Campeloma sp........... D July 4 37 0 0 0 
Lymnaea stagnalis....... S July 7 30 0 0 0 
Lymnaea emarginala..... H July 8 28 0 1 (Cercaria sp.) 325 
Lymnaea stagnalis....... H July 8 8 1 (Stylet) 1 (C. elvae) 12.5 
var. appressa 
Planorbis bicarinata H July 8 9 1 (Stylet) 0 0 
Campeloma decisum...... H July 8 24 0 0 0 
Lymnaea stagnalis. ...... M july 8 5 0 0 0 
var. perampla 
Lymnaea stagnalis....... M july 8 2 0 0 0 
var. appressa 
Lymnaea emarginata..... M july 8 16 0 0 0 
PHYSORG. 05s acne so M july 8 1 0 0 0 
Campeloma sp. ......... M july 8 1 0 0 0 
Planorbis trivolvis........ M July 8 3 0 0 0 
Planorbis trivolvis........ S July 20 37 0 1 (C.elephantis) 2.7 
PRYS@1OPEG 3 dees emai Get « H July 20 20 0 2 (Cercariasp.) 10.0 
Lymnaea stagnalis. ...... M July 22 27 0 2 (C. douthitti) 7.4 
var. appressa 
Planorbis bicarinata...... M july 22 20 0 0 0 
Lymnaea megasoma...... T July 24 35 0 0 0 
Lymnaea stagnalis....... B Aug. 4 23 0 1 (C. elvae) 4.3 
var. appressa 
Physa lordi............. B Aug. 4 1 0 0 0 
Lymnaea megasoma...... Cc Aug. 9 18 0 1 (C. chrys- 5.5 
enterica) 
Lymnaea sp............. C Aug. 9 3 0 0 0 
Planorbis trivolvis........ C Aug. 9 73 2(Echinos- 2 (C. tenuis) 2.7 
tome) 7 (C. burti) 9.6 
2 (Stylet) 1 (C. rhab- 1:3 
docaeca?) 


B, Bessey Creek; C, Colonial Point, Burt Lake; D, Laboratory Dock; H, Hook Point; 
M, Maple River; S, Sedge Pond; T, Topinabee Road Pool. 


341] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER_ 83 


TABLE IIT 


Collection record for 1921-1922; vicinity of Urbana, Illinois. 
All snails were isolated for emerging cercariae and subsequently crushed to find im- 
mature infections (furcocercous and other). 


n 
20 o og O YO 
eee ss5sesegsea 
pecies of BEOeSe EEE 
snail Place Date No. All infections a A AA A 
Physa gyrina...... D = Sept.18 97 2 (C. multicellulata) 221).0 2.1 0 2.4 
Planorbis trivolvis.. D  Sept.18 24 0 0 0 0 0 0 
Physa gyrina...... D ‘Sept.28 71 2 (C. gigas) 2.8 0 2.8 0 2.8 
Planorbis trivolvis.. D Sept. 28 103 1 (C. hamata) 1.0 0 1.0 0 1.0 
Physa gyrina...... D Oct. 21 15 O 0 0 0 0 0 


Planorbis trivolvis.. D Oct. 21 60 6 (Stylet, mature) 

5 (Stylet, immature) 0 18.0 10.0 8.0 18.0 
Physa gyrina...... D Oct. 24 102 2 (C. gigas) 

3 (Stylet, mature) 

4 (Stylet, immature) 2.0 7.0 5.0 4.0 9.0 
Planorbis trivolvis.. D Oct. 24 31 5 (Stylet, mature) 

3 (Stylet, immature) 0 25.8 16.1 9.7 25.8 
Physa gyrina......_ D Oct. 26 180 1 (Monostome, mature) 

2 (Stylet, mature) 

1 (Stylet, immature) 0 D2 teh (OS: Zee 
Planorbis trivolvis... D Oct. 26 101 1 (C. hamata) 

14 (Stylet, mature) 

6 (Stylet, immature) 

4 (Cercariasp.immat.) 1.0 23.8 13.8 10.0 24.8 


Physa gyrina...... S) Oct. 31. 23: 0 0 0 0 0 0 
Planorbis trivoluis.. M Nov. 1 9 O 0 0 0 0 0 
Physa gyrina...... C Nov. 4 81 0 0 0 0 0 0 
Physa gyrina...... D Nov. 4 177 12 (C. multicellulata) 6.8 0 6.8 0 6.8 
Planorbis trivolvis.. D Nov. 4 11 1 (C. kamata) 

1 (Stylet, mature) 0.9 0.9 1.8 0 1.8 


D, Drainage Ditch; C, Campus Stream; M, Pond at Muncie, Illinois; S, Spoon River, 
St. Joseph, Illinois. 


Miscellaneous 
These snails were isolated for emerging cercariae; they were not subsequently crushed. 
Gonionasis sp. Olentangy River, Ohio Sept. 1921 200 individuals Negative 
Gonionasis laqueata Brown’s Creek, Nashville, Tenn. Feb. 1, 1923 378 individuals Negative 


S4 ILLINOIS BIOLOGICAL MONOGRAPHS (342 


SUMMARY OF RESULTS 


1. The furcocercous larval trematode fauna of restricted regions of 
Illinois and of Michigan has been studied. 

2. Seven new species (Miller, 1923) have been here fully described in 
comparison with morphologically similar cercariae. 

3. The literature for one hundred and two fresh-water, and for eight 
marine species of furcocercous cercariae has been reviewed and summa- 
rized; a check list is submitted. 

4. Of the new species, the two apharyngeal distomes make clear the 
establishment of two well-defined groups. 

5. The three pharyngeal longifurcate distomes add to the knowledge of 
this group, in which there are but few complete descriptions. 

6. The two longifurcate monostomes, both probably pharyngeal, make 
possible the formation of a group of these forms. 

7. Studies carried on to supplement incomplete descriptions of certain 
North American larvae have made possible their more exact disposition. 

8. It has been possible to make a satisfactory scheme of classification, 
based largely on the excretory system, for only the apharyngeal brevifur- 
cate distomes. 

9. The importance of the excretory system in the determination of 
relationships is stressed; but due emphasis has also been placed on other 
features of morphology. 

10. From a resume of the literature it is clear that in addition to the 
Schistosomatidae some members, and probably all, of the Holostomata 
develop from furcocercous larvae; so also does Sanguinicola inermis of the 
Aporocotylidae. 


343] COMPARATIVE STUDIES ON FURCOCERCOUS CERCA RIAE—MILLER 85 


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Faust, E. C. 

1917. Notes on the cercariae of the Bitter Root Valley, Montana. Jour. Parasit., 
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1918, Life history studies on Montana trematodes. Ill. Biol. Monogr., 4:1-120; 9 pl. 

1918a. Studies on Illinois cercariae. Jour. Parasit., 4:93-110; 2 pl. 

1918b. Eye-spots in Digenea. Biol. Bull., 35:117-127; 3 text-figs. 

1918c. The anatomy of Tetracotyle iturbet Faust, with a synopsis of described tetra- 
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1919. A biological survey of described cercariae in the United States. Amer. Nat., 
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1919a. Notes on South African cercariae. Jour. Parasit., 5:164-175; 1 pl. 

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1919c. The excretory system in Digenea. II. Observations on the excretory system in 
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1919d. The excretory system in Digenea. III. Notes on the excretory system in a 
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1920. Pathological changes in the gasteropod liver produced by fluke infection. Johns 
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1920a. Criteria for the differentiation of schistosome larvae. Jour. Parasit., 6:192-194; 
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1920b. A survey of Cawston’s species of South African cercariae. Parasitol., 12:212-216; 
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1921. Larval flukes from Georgia. Trans. Amer. Micr. Soc., 40:49-58; 2 pl. 

1921a. The excretory system in Digenea. IV. A study of the structure and develop- 
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1921b. The present state of the schistosome problem. China Med. Jour., 35:405-410. 

1921c. Recent advances in parasitology. Trans. Amer. Micr. Soc., 40:75-88. 

1921d. Notes on South African larval trematodes. Jour. Parasit., 8:11-21; 1 pl. 

1922. Phases in the life history of a holostome, Cyathocotyle orientalis nov. sp. With 
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1922a. Notes on larval flukes from China. Parasitol., 14:248-267; 2 pl. 

1924. Notes on larval flukes from China. II. Studies on some larval flukes from the 
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88 ILLINOIS BIOLOGICAL MONOGRAPHS (346 


Faust, E. C., and MEteEny, H. E. 

1923. Studies on schistosomiasis japonica: Morphology, biology and life history of the 
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3 


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347] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 89 


Kopayasai, H. 
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Manson-Banr, P., and Farriry, N. H. 
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1920. Physiological Chemistry. 1154 pp. 
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349] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 91 


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1917. Larval trematodes from Kansas fresh-water snails. Kansas Univ. Sci. Bull., 

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1862. Untersuchungen iiber niedere Seethiere aus Cette. Zeitschr. wiss. Zool., 12: 

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1894. L’elmintologia italiana da suoi primi tempi all’anno 1890. Storia, sistematica, 

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1906. Trématodes parasites de mollusques marins. Bull. sci. France et Belg., 40: 

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1905. Sanguinicola armata und inermis (n. g., n. sp.), n. fam. Rhynchostomida. Ein 
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8 figs. 

1908. Ein monozoischer Cestode als Blutparasit (Sanguwinicola armata und inermis 
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PorTER, A. 

1920. The experimental determination of the vertebrate hosts of some South African 
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1920a. The invertebrate (molluscan) hosts of Schistosoma mansoni and Fasciola hepatica 
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1909. On Holostomum excisum (Linstow, 1906), and the development of a tetra- 

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SCHEURING, L. 

1920. Die Lebensgeschichte eines Karpfenparasiten (Sanguinicola inermis Plehn). 
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1918. Parasites of Indian fishes, No. 5. Rec. Ind. Mus., 15:341-355; 5 pl. 
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1921. A new blood fluke from turtles. Jour. Parasit., 7:114-128; 1 pl. 
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1918. Fresh-Water Biology. 1111 pp., 1547 text-figs. 
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1917. Onthe cercariae in Melania. Zool. Mag., 29:103-119 [Japanese]. 


94 


ILLINOIS BIOLOGICAL MONOGRAPHS 


EXPLANATION OF PLATES 


Unless otherwise stated, all drawings were made with the camera lucida. 
Abbreviations used: 


ao 
bp 
ic 
ct 
d 
da 
dp 
e€ 
es 


anterior organ 

birth-pore 

cecum 

caudal excretory tube 
penetration gland duct 

anterior penetration gland duct 
posterior penetration gland duct 
esophagus 

pigmented eye-spot 


gb 
ge 
hg 


germ ball 

germ cells 

head gland 

muscle band 

nervous system 

penetration gland cell 

anterior penetration gland cell 
posterior penetration gland cell 
ventral sucker 


[352 


353] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 95 


PLATE I 


96 


ONE RS 


ILLINOIS BIOLOGICAL MONOGRAPHS {354 


DESCRIPTION OF PLATE I 
All figures concern Cercaria multicellulata 


Diagrammatic view of ventral side, showing probable connections of excretory 
system. X 760 

End of sporocyst, showing birth-pore. 760 

Ventral view. 310 

Diagrammatic outline to show annulations of body. X 365 

Ventral view, showing excretory system in relation to other organs. 760 
Transverse section of tail-stem, showing four muscle fields, and caudal excretory 
tube. X 630 

Almost median sagittal section. > 740 


VOLUME X 


ILLINOIS BIOLOGICAL MONOGRAPHS 


Og 
peo 
U0. 


9 
[oF 
9 
Seto! 


2) Bo, 


PLATE I 


MILLER 


THE LIBRARY 


ge THE 


355] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 97 


PLATE II 


98 


Fig. 


Fig. 
Fig. 
Fig. 
Fig. 
Fig. 
Fig. 
Fig. 
Fig. 
Fig. 
Fig. 


ILLINOIS BIOLOGICAL MONOGRAPHS 


DESCRIPTION OF PLATE II 


Cercaria multicellulata; transverse section through posterior penetration glands. 


x 740 
Figs. 9 to 16 inclusive concern Cercaria hamata 


. Transverse section through anterior organ. XX 975 

. Transverse section through tail-stem. > 775 

. Outline of living sporocyst containing early germ balls. X 60 
. Semi-diagrammatic ventral view. X 390 

. Outline of club-shaped end of living sporocyst. X 75 

. End of sporocyst showing birth-pore. X 75 

. Transverse section through young sporocyst. > 375 


Transverse section through anterior germ cell mass. X 1000 


. C. multicellulata; transverse section through pigmented eye-spots. 
. C. multicellulata; outline of living sporocyst. X 42 


X 620 


ILLINOIS BIOLOGICAL MONOGRAPHS VOLUME X 


MILLER PLATE II 


= 
eo 

=< 

os 
[= =3 
—_ 


ted - 
ms 
te 
| ee 
ee 


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357] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 99 


PLATE HI 


100 


Fig. 
Fig. 
Fig. 
Fig. 
Fig. 
Fig. 
Fig. 


19. 
20. 
21. 
22s 
23. 
24, 
25. 


ILLINOIS BIOLOGICAL MONOGRAPHS 


DESCRIPTION OF PLATE III 


All figures concern Cercaria elvae 
Dorsal view of body. X 410 
Ventral view of excretory system. X 410 
Lateral view of body. X 400 
Outline of anterior organ, as frequently seen in living animal. X 135 
Transverse section through tail-stem. > 560 
Furcal tip, dorsal view. X 115 


Semi-lateral view of body characteristic of living larva under cover glass. 


[358 


VOLUME X 


ILLINOIS BIOLOGICAL MONOGRAPHS 


PLATE III 


MILLER 


THE LIBRARY 
OF THE 


Gane 


359] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 101 


PLATE TY 


102 


‘ig. 41. 


- 42, 


ILLINOIS BIOLOGICAL MONOGRAPHS [360 


DESCRIPTION OF PLATE IV 


. Cercaria elvae; transverse section through anterior organ just in front of mouth, 


showing head gland and penetration gland ducts. X 550 


. C. elvae; transverse section through tip of anterior organ. > 480 
. C. elvae; transverse section through posterior end of anterior organ, showing in 


addition the esophagus. X 450 

. wardi; body outline of living animal frequently observed. > 100 

. wardi; lateral view of excretory system. > 190 

wardi; ventral view of excretory system. X 180 

. wardi; lateral view of body, with details of structure. > 270 

wardi; body outline of living animal frequently observed. X 110 
wardi; outline of everted ventral sucker, showing spination. 285 
wardi; outline showing furcal fin-folds from dorsal view. X 145 

. wardi; ventral view of body, with details of structure. > 250 

. wardi; outline showing posterior mucin gland in lateral aspect. X 85 
. elvae; outline of transverse section through ventral sucker region, showing that 
organ retracted into body. X 315 


anaaaaaaaa 


. C. elvae; transverse section through lateral eye-spots, showing also esophagus, an 


anterior penetration gland, and the five pairs of penetration gland ducts. X 430 


. C.elvae; transverse section through ventral sucker, showing anterior penetration 


glands (ventral) and ducts (dorsal) from posterior penetration glands. X 445 

C. elvae; transverse section through nervous system, showing esophagus and penetra- 
tion gland ducts. & 485 

C. elvae; transverse section through penetration glands and germ cell mass. X 450 


VOLUME X 


ILLINOIS BIOLOGICAL MONOGRAPHS 


PLATE IV 


MILLER 


THE LIBRARY 
OF THE 


Romine daratn 
Ks nda 


if 


361] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 103 


PLATE V 


104 


Fig. 


Fig. 
Fig. 


Fig. 
Fig. 
Fig. 
Fig. 
lig. 
Fig. 
Fig. 


Fig. 
Fig. 


43. 


53. 
54. 


ILLINOSI BIOLOGICAL MONOGRAPHS [362 


DESCRIPTION OF PLATE V 


Cercaria wardi; transverse section through head gland, penetration gland ducts, 
and esophagus in anterior organ. X 710 


. C. wardi; lateral view. X 75 
. C. wardi; transverse section through tail-stem, showing caudal excretory tube and 


muscles. X 555 


. C. burti; median sagittal section through immature larva. XX 460 

. C. burti; portion of sporocyst. XX 30 

. C. burti; end of sporocyst, showing birth-pore. XX 70 

. C. burti; transverse section through ventral sucker, showing ceca and penetration 


gland ducts. X 580 


. C. wardi; transverse section through ventral sucker, showing both types of penetra- 


tion gland cells. > 525 


. C. wardi; transverse section through furca, showing prominent furcal fin-folds. 


x 750 


. C. wardi; transverse section through eye-spots of immature specimen, showing 


esophagus, nerves, and penetration gland ducts. X 770 

C. wardi; portion of a sporocyst, drawn from living material. X 60 

C. wardi; transverse section through germ cell mass, dorsal posterior mucin gland, 
and two penetration gland cells. X 430 


ILLINOIS BIOLOGICAL MONOGRAPHS VOLUME X 


MILLER PLATE V 


THE LIBRARY 


363] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 105 


PLATE VI 


106 ILLINOIS BIOLOGICAL MONOGRAPHS [364 


DESCRIPTION OF PLATE VI 


Fig. 55. Cercaria burti; transverse section through anterior organ. > 600 

Figs. 56, 57, 58. C. burti; form changes of body of living animal. 

Fig. 59. C. tenuis; transverse section through tail-stem. X 520 

Fig. 60. C. tenuis; transverse section through penetration glands. 560 

Fig. 61. C. tenuis; portion of sporocyst showing birth-pore. > 45 

Fig. 62. C. burti; ventral view showing relations of alimentary canal, penetration glands, 
nervous system, and germ cell mass. X 500 


Fig. 63. C. burti; ventral view of excretory system. X 480 

Fig. 64 burti; transverse section through germ cell mass. XX 525 
Fig. 65. C. burti; outline sketch showing intestinal ceca. XX 375 
Fig. 66 burti; ventral view, showing general appearance. X 245 


tenuis; transverse section through ventral sucker. > 795 

tenuis; transverse section through tail-stem. > 865 

. tenuis; general appearance from ventral view. X 160 

tenuis; transverse section through anterior organ. 840 

. tenuis; spine from ventral sucker, free-hand drawing. X about 2250 


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ILLINOIS BIOLOGICAL MONOGRAPHS VOLUME]X 


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365] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 107 


PLATE VII 


108 


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Fig. 
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ILLINOIS BIOLOGICAL MONOGRAPHS 


DESCRIPTION OF PLATE VII 


. Cercaria tenuis; longitudinal section through sporocyst. > 595 
enGs 


tenuis; transverse section through sporocyst. XX 280 

tenuis; ventral view of excretory system in body. X 410 

tenuis; semi-diagrammatic ventral view. X 410 

tenuis; transverse section through penetration gland region. XX 865 
tenuis; end of sporocyst showing birth-pore. XX 255 

chrysenterica; ventral view. X 390 

chrysenterica; ventral view of excretory system. XX 220 


. chrysenterica; free-hand drawing of spine from oral cap. 
. chrysenterica; transverse section through furca. X 635 


[366 


ILLINOIS BIOLOGICAL MONOGRAPHS VOLUME X 


MILLER PLATE VII 


QUITE ERSHTY 6 


THE LIBRARY 
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367] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 109 


PLATE VIII 


110 


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Fig. 


Fig. 
Fig. 


Fig. 


ILLINOIS BIOLOGICAL MONOGRAPHS [368 


DESCRIPTION OF PLATE VIII 


All figures concern Cercaria chrysenterica 


82, a-f. Outlines of developmental stages. > 105 


83. 
. Transverse section through level a—a of Fig. 78. X 915 

. General appearance of an entire sporocyst. XX 15 

. Transverse section through level c—c of Fig. 78. > 730 

. Transverse section through sporocyst, showing cercariae in all stages of develop- 


or 


End of sporocyst, showing birth-pore. X 155 


ment. X 220 


. Transverse section through distal end of tail-stem, showing caudal excretory tube 


divided to pass down each furca. XX 705 


. Transverse section through level b—b of Fig. 78. > 730 
. Transverse section through young sporocyst, anterior end of contained cercaria, 


and germ ball. > 565 
Outline of tail-stem of living larva, as often held when under a cover glass. > 45 


Figs. 92, 93,94. Form changes of body of the living animal under a cover glass. 


ILLINOIS BIOLOGICAL MONOGRAPPS VOLUME X 


MILLER PLATE VIII 


THE LIBRARY 


pany? ERSITY QP tat 
Whioy GUwCod © car 


369] COMPARATIVE STUDIES ON FURCOCERCOUS CERCARIAE—MILLER 111 


INDEX OF SCIENTIFIC NAMES 


gladii, 15, 45, 69, 75 

gracilis, 8, 23, 71, 77 
gracillima, 13, 22, 28, 50, 69, 75 
eyrinipeta, 71, 75, 77, 79 

H (Kobayashi), 75 

hamata, 50, 55, 70, 75 

of Haplocladus minor?, 11, 80 
in Haswell 1902, 26 

of Hemistomum alatum, 70, 75 
in Hesse 1923, 71, 75 

I (Kobayashi), 75 


Agamodistomum marcianae, 15, 79 
Aporocotyle, 18 
Aporocotylidae, 22, 79, 84 
“Bilharziella”, 30, 66 
Bithynia tentaculata, 16 
Bullinus, 12, 25 
Campeloma, 7 

Campeloma decisum, 82 
Campeloma rufum, 82 
Campeloma sp., 82 
Cercaria A (Kobayashi), 74 


A (Szidat), 23, 70, 80 

aculeata, 9, 71 

sp. LX (Ando), 74 

sp. X (Ando, 75 

andoi, 73 

B (Kemp), 14, 65, 74 

B (Kobayashi, 74 

B (Szidat), 23, 71 

VI (von Baer), 8, 74 

bdello cystis, 71, 77 

bilharziella, 12, 17, 61, 74 
bilharziella lunata, 18, 74 
bipartita, 10, 74 

in Blacklock and Thompson, 64, 74 
blanchardi, 2, 65, 74 
bombayensis no. 8, 19, 62, 68, 74 
bombayensis no. 9, 19, 61, 74 
bombayensis no. 13, 19, 35, 74 
bombayensis no. 19, 24, 30, 66, 74 
burti, 41, 46, 71 

C (Kemp), 18, 65, 74 

C (Kobayashi), 74 

C (Szidat), 23, 71 

chrysenterica, 45, 47, 71 

crispa, 17, 21, 65, 74 

cristata, 8, 18, 68, 74, 78 

D (Kobayashi), 75 

dichotoma, 8,77 

discursata, 11, 28, 77 

divaricata, 23, 61, 71 
divaricauda, 75 

douglasi, 13, 41, 71, 78 

douthiiti, 11, 16, 22, 30, 38, 52, 65, 75, 82 
E (Kobayashi), 75 

echinocauda, 13, 22, 31, 67, 81 
elephantis, 13, 16, 20, 24 

elvae, 24, 30, 35, 39, 48, 65, 75, 82 
emarginatae, 13, 16, 47, 71, 79 
F (Kobayashi), 15, 75 
Sissicauda, 8, 21, 71, 80 

Surcata, 8, 23, 73, 77 

furcicauda, 15, 71, 75 

G (Yoshida), 13, 75 

gigantea, 23, 30, 66, 75 

gigas, 14, 17, 38, 53, 61, 75 


indica I, 71, 75 
TT, 56;/71,.75. 
IX, 56, 61, 68, 75 
XIII, 56, 68, 75 
XV, 20, 72, 75 
XXII, 43, 60, 69, 75 
XXV, 34, 35, 60, 75 
XXVII, 51, 56, 69, 75 
XXX, 16, 25, 30 
XXXII, 72, 75 
XXXVI, 60, 67, 75 
XXXIX, 56, 68, 75 
XLVII, 61, 65, 75 
LV, 56, 61, 68, 75 
LVIII, 72, 75 
inhabilis, 81 
inversa, 13, 73, 76 
J (Kobayashi), 75 
sp. no. 1 in. Lagrange 1919, 73, 76 
in Lagrange 1923 : 175, 69, 76 
in Lagrange 1923 : 177, 73, 76 
in Leiper 1925; text-fig. 46, 12, 76 
in Leiper and Atkinson 1915, 12, 72, 76 
leptoderma, 21, 28, 72, 76 
letifera, 13, 23, 47, 52, 72, 79 
in Linton 1915, 76 
in Linton 1915a, 76 
longissima, 72 
in Lithe 1909 : 204, 73, 76 
Liithe 1909 : 206, 73, 76 
in Manson-Bahr and Fairley 1920 
Pi. II, fig. 5, 17, 65, 73, 76 
in Manson-Bahr and Fairley 1920 
Pl. III, fig. 7, 73, 76 
marcianae, 13, 76, 79 
microcristata, 9, 68, 76 
minima, 15, 69, 76 
minor (Faust), 14, 76 
minuta, 9,72, 76 
molluscipeta, 72, 76, 79 
in Morgan 1891, 77 
multicellulata, 42, 50, 70, 76 
sp. XIV (Nakagawa), 76 
sp. XV (Nakagawa), 76 
ocellata, 8, 30, 66, 76, 77 


112 ILLINOIS BIOLOGICAL MONOGRAPHS [370 


ocellifera, 73, 76 Histrionellina fissicauda, 9, 77 
octadena, 19, 70, 76 Holostomata, 79, 84 
oculata, 14, 18, 67, 76 Hydroides, 13 
paludinarum, 73, 76 Hydroides dianthus, 12 
parthenicola, 70, 76 Isidora, 25 
parvoculata, 15, 68, 76 Isidora tropica, 19 
patialensis, 68, 76 Lophocercaria fissicauda, 9, 77 
pseudo-divaricata, 73, 76 Lymnaea, 25 
pseudo-vivax, 23, 61, 72 Lymnaea acuminata, 30 
quatluor-solenata, 15, 72, 76 auricularia, 78 
quieta, 13, 73, 76 emarginata, 82 
redicola, 72, 76 megasoma, 7, 50, 82 
rhabdocaeca, 15, 50, 55, 72, 82 natalensis, 17 
robusticauda, 15, 61, 72, 76 palustris, 23, 80 
of Sanguinicola inermis, 68, 76 peregra, 22 
of Schistosoma haematobium, 12, 16, 25,35, 64, reflexa, 30 
76 stagnalis, 82 
of Schistosoma japonicum, 11, 28, 30, 38, 61, var. appressa, 30, 35, 82 
64, 76 var. perampla, 82 
of Schistosoma mansoni, 11, 16, 24, 34, 38, 65, sp., 82 
77 Malleolus, 8 
of Schistosoma spindale, 15, 18, 30, 65, 77 Malleolus furcatus, 8, 77 
of Schistosomatium pathlocopticum, 38, 65, 77 Pecten irradians, 13 
scripta, 70, 77 Physa, 7 
secobiana, 14, 78 Physa ancillaria, 41 
secobti, 12, 19, 72, 77 gyrina, 50, 54, 81 
in Seno 1903, 87 : lordi, 81 
senot, 73, 77 Physopsis, 25 
shinchikuensis, 73, 77 Physopsis africana, 12, 17 
spinosa, 15, 18, 65, 77 cf. globosa, 24 
in Suzuki and Nishio 1914, 77 Planorbis, 7, 17, 25, 79 
syndosmyae, 10, 77 Planorbis bicarinata, 82 
tenuis, 45, 72, 77, 82 boissyi, 12 
tuberistoma, 13, 69, 77 metidjensis, 25 
valdefissa, 73, 77 pfeifferi, 18 
varicans, 8, 68, 73, 77 Srivolvis, 20, 35, 41, 55, 81 
vergrandis, 13, 79 Proparorchiidae, 18 
vivax, 9, 21, 60, 72, 80 Sanguinicola, 18, 79 
wardi, 30, 35, 47, 66, 77, 82 Sanguinicola inermis, 18, 21, 68, 77, 84 
C. (Schizocerca) dichotoma, 9, 77 Schistocercaria, 19, 77 
C. (Schizocerca) fissicauda, 9, 77 Schistosoma, 12, 22 
C. (Schizocerca) gracilis, 9, 77 Schistosoma bovis, 70 
Cheilostomum, 8 haematobium, 12, 16, 25, 30, 38, 61, 76 
Cheilostomum varicans, 8, 77 japonicum, 11, 30, 38, 61, 76 
Dicranocercaria bdellocystis, 18, 77 mansoni, 11, 16, 24, 34, 65, 77 
gyrinipeta, 18, 77 spindale, 15, 30, 65, 77 
molluscipetd, 18, 77 Schistosomatidae, 18, 22, 30, 62, 78, 84 
ocellifera, 17 Schistosomatium pathlocopticum, 22, 38, 66, 77 
valdefissa, 17 Spirorchidae, 22, 62, 79 
Echinostomum revolutum, 81 Strigea, 18, 79 
Goniobasis, 7 Strigea tarda, 80 
Goniolasis laqueata, 83 Syndosma alba, 10 
Goniobasis sp., 83 Tetracotyle typica, 23, 70, 80 
Gyraulus euphraticus, 18 Thamnophis eques, 79 
Haplocladus minor, 11, 77 marcinia, 79 
Hemistomum alatum, 21, 70, 78, 79 Tylodelphis, 21, 80 
Histrionella fissa, & Vibrio, 8 


Histrioneliina, 9 Vibrio malleus, & 


i 


01 12 065097252 


